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Available online at www.nznaturalsciences.org.nz Same enemy, same response: predator avoidance by an invasive and native snail Joseph R. Holomuzki1,3 & Barry J. F. Biggs2 1Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, Mansfield, Ohio, U.S.A. 2National Institute of Water and Atmospheric Research Limited, Christch- urch, New Zealand 3Corresponding author’s email: [email protected] (Received 21 December 2011, revised and accepted 25 April 2012) Abstract Novel or highly effective antipredator traits can facilitate successful invasions by prey species. Previous studies have documented that both the native New Zealand snail, Potamopyrgus antipodarum, and the highly successful, worldwide invader Physella (Physa) acuta, seek benthic cover to avoid fish predators. We asked whether an invasive, South Island population of Physella has maintained this avoidance response, and if so, how it compared to that of Potamopyrgus that has coevolved with native fish. We compared patterns of sediment surface and subsurface use between snail species and between sizes of conspecifics both in a 2nd –order reach with predatory fish and in a laboratory experiment where fish presence (common bullies [Gobiomorphus cotidianus]) was manipulated. Both snails sought protective sediment subsurfaces when with bullies. Proportionally, sediment subsurface use both in field collections and in fish treatments in the experiment were similar between species. Field-captured bullies ate more Physella than Potamoprygus, suggesting different consumptive risks, but overall, few snails were consumed. Instream densities and sizes (shell length) of Physella were greatest on cobbles, where most (>90%) egg masses were found. Potamopyrgus densities were evenly distributed across sand, gravel, and cobbles. Shell lengths were similar between snails on sediment subsurfaces and surfaces during daylight for both species, suggesting this avoidance response was not size-dependent. For Physella, retaining the ability to seek benthic refugia when exposed to novel predators likely greatly contributes to its invasion success. Given both snails are dominant primary consumers in many freshwater ecosystems, surface-density increases resulting from predation pressure decreases would predictably significantly affect system trophic dynamics. Key words: bully predation – Physella acuta – Potamopyrgus antipodarum – sediment surface and subsurface use – shell length – sediment size New Zealand Natural Sciences (2012) 37: 11-24. © New Zealand Natural Sciences 12 New Zealand Natural Sciences 37 (2012) Introduction hence displace other macroinvertebrates and fish (Lowe & Hunter 1988; Win- Novel or highly effective antipredator terbourn & Fegley 1989; Biggs & Lowe traits can facilitate successful invasions 1994). In New Zealand, their popula- by prey species. Traits that allow benthic tions seldom reach high densities, in part macroinvertebrate invaders to effectively because of predation by native and non- deter or avoid native predators, and hence native fishes (Levri 1998; Holomuzki & to become successful, include armouring Biggs 2006; Holomuzki 2010). (spines) (Zaranko et al. 1997; Levri et Predation risk might be a key driver al. 2007), inedibility (Strayer 2009), of microspatial patterns of both snails. activity reductions (Pennuto & Keppler Potamopyrgus generally resides on a 2008), and movement to spatial refugia broad range of sediment sizes (Jowett et (Dalesman et al. 2007). Identifying and al. 1991), but in streams, is most dense assessing the relative effectiveness of on cobbles in slow current speeds (≤ antipredator traits of native and non- 15 cm/s) (Holomuzki & Biggs 2007). native prey is important to predicting Regardless of sediment size, in streams the potential rate and geographical extent with predatory fish, ~80% of all Pota- of invader spread and impacts on native mopyrgus occur in sediment subsurfaces species numbers and assemblages (Levine with limited predator access (Holomuzki et al. 2003; Temperton et al. 2004). et al. 2009). Moreover, Potamopyrgus This study compares predator avoid- will move to protective sediment sub- ance behaviours by a native and non- surfaces when in the presence of mol- native snail. Potamopyrgus antipodarum luscivorous bullies (Gobiomorphus spp.), (Gray 1843) is native to New Zealand a widespread native fish in New Zealand streams and lakes, where it commonly streams and lakes (Holomuzki & Biggs co-exists with the highly successful, 2006). Similarly, Physella acuta will worldwide invader Physella (Physa) acuta move under cover when in the physical (Draparanaud 1805) (McCarter 1986; or chemical presence of pumpkinseed Cope & Winterbourn 2004; Kristensen sunfish (Lepomis gibbosus) (Turner 1996; & Closs 2008), apparently introduced Turner & Montgomery 2003) and creek from the Mediterranean region of Europe chub (Semotilus atromaculatus) (Turner or North America ca. 40 years ago (Win- et al. 2000), important molluscivores in terbourn 1973). Potamopyrgus is now also eastern North America (Brönmark et al. found in southeastern Australia (Sch- 1992). However, for invasive populations reiber et al. 1998; 2003), Japan (Shimada in New Zealand, it is unclear whether & Urabe 2003), Europe (Statzner 1981), Physella has retained this response, and the Laurentian Great Lakes (Zaranko et how this response, if retained, compares al. 1997), and the western United States to predator-induced microspatial shifts (Dybdahl & Kane 2005). So, both snails by Potamopyrgus that has coevolved with also widely co-occur as non-native spe- native predators. cies. When at high densities or biomass, The magnitude of any avoidance re- grazing by both snails can significantly sponse might also depend on predation reduce algal biomass and richness, alter risk and prey vulnerability. Bullies eat algal physiognomy and composition, and both Physella and Potamopyrgus (Sagar Holomuzki & Biggs: Predator avoidance by invasive and native snails 13 & Glova 1995; Wilhelm et al. 2007), snail size distributions. but it is unknown whether consumptive risk from bullies differs between these Methods snails. Non-native, young brown trout (Salmo trutta) in New Zealand streams Snail and sediment field sampling apparently eat similar numbers of Pota- mopyrgus and Physella (Holomuzki 2010), Snails were sampled in the East Branch of even though Physella is larger-bodied the Kaiapoi River (a.k.a. Silverstream; lat (~7 mm average length), softer-shelled, 43.25°S, long 172.35°E) 26 km north of and energetically more profitable than Christchurch on 1 and 2 February 2011. Potamopyrgus (4–6 mm average length) Snails were collected in a ~25-m-long, (McCarter 1986). Moreover, in North ~11-m-wide reach (current velocity: America, Physa integra (= P. acuta, Dillon 5–16 cm/s; water depths: 12–31 cm) et al. 2002) are smaller at sites with fish containing mainly coarse gravel to small than without fish (Bernot & Whittinghill cobbles armouring sand. Macrophytes, 2003), but it is unclear if snails are smaller mostly watercress (Nasturtium officinale), because of size-selective predation or be- were present only along shorelines. The cause larger snails exhibit stronger avoid- predominant fishes in this 2nd-order ance behaviours that reduce predation reach were common bullies, short-finned risk than smaller ones. For Potamopyrgus, eels (Anguilla australis), and brown trout small, non-parasitized individuals (<3.8 (Holomuzki & Biggs, 2006). Indigenous mm length) are more active than large Paranephrops zealandicus crayfish were individuals on tops of rocks during day- absent (JRH, pers. obs.). light (Levri & Lively 1996), suggesting The reach was mapped to create a grid predation risk might vary with body size. system for sampling snails and sediments. Here, we present results from field The grid contained 2 rows, each 1-m wide collections, gut-evacuation observations, and 5 m-long near mid-channel, and and a laboratory experiment to examine spaced 1-m apart. Each row was divided 1) how densities of each snail vary with into twenty 0.5 x 0.5 m plots. Plots were sediment size, 2) how patterns of sedi- used to collect snails and sediments, and ment subsurface use differ between Phy- the 1-m wide space between the rows sella and Potamopyrgus and between sizes in the middle of the reach served as a of conspecifics when with predatory fish, walkway to minimize disturbance in and 3) whether these snails are equally sample plots. Twenty one of the 40 plots important prey items for common bul- within the grid were randomly selected lies (Gobiomorphus cotidianus McDow- for sampling with a cylindrical stovepipe all). Microdistributional patterns of P. core sampler (40 cm height, 25.4 cm di- acuta in streams are unknown, but clearly ameter). The sampler was pushed ~5 to 15 important to understanding trophic cm into sediments and all snails and sedi- relationships. We also relate egg mass dis- ments within the sampler were collected. tributions to sediment sizes for Physella, However, collection procedure varied but not for ovoviviparous Potamopyrgus, with water depth at plots. In depths <25 because egg-laying habitat preferences cm, all epibenthic snails in the sampler might affect sediment use patterns and were removed by suctioning, then sedi- 14 New Zealand Natural Sciences 37 (2012) ments were removed with a dip net (0.5 x 10 in the laboratory between north- and 0.5-mm mesh) to a depth of ~5 to 15 cm. west-facing windows to expose fish to a In depths from ~25 to 31 cm, epibenthic natural