The timing of Carcinus maenas recruitment to a south ...

Author's personal copy Hydrobiologia DOI 10.1007/s10750-015-2332-z

PRIMARY RESEARCH PAPER

The timing of Carcinus maenas recruitment to a south-east Australian estuary differs to that of native crabs C. J. Garside . T. M. Glasby . L. J. Stone . M. J. Bishop

Received: 4 November 2014 / Revised: 14 March 2015 / Accepted: 17 May 2015 Ó Springer International Publishing Switzerland 2015

Abstract Strong seasonal trends in reproduction and early development of many invasive species are commonplace and may differ between introduced and native ranges, reflecting differences in abiotic conditions that trigger reproduction, or in selective pressures. The invasive crab Carcinus maenas has been present in south-east Australia for over 100 years, but little is known about its recruitment to benthic substrates in this introduced range. This study assessed the timing of C. maenas and native crab recruitment to Merimbula Lake (36.89oS, 149.92oE) south-eastern Australia between August 2011 and October 2013. It also assessed the effectiveness of four different types of recruitment bags for detecting the invasive crab. Carcinus maenas recruited in greater numbers to bags that contained live oysters than those with oyster shell, artificial turf or without structure. Recruitment of C. maenas peaked in the late winter and spring, while recruitment of most native species peaked in autumn. The timing of C. maenas recruitment contrasted its native European range where

Handling editor: Alison King C. J. Garside (&) L. J. Stone M. J. Bishop Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia e-mail: [email protected] T. M. Glasby NSW Department of Primary Industries, Port Stephens Fisheries Institute, Taylors Beach, NSW 2316, Australia

recruitment typically occurs in summer and autumn. Although likely triggered by the warmer water temperatures of south-eastern Australia, this differing reproductive phenology of C. maenas between its native and Australian range may also modify its interactions with native crab recruits. Keywords Invasive Non-indigenous Crab Seasonal Phenology Reproductive Temperature

Introduction The process of biological invasion requires the longdistance transportation of species to new locations (introduction), their establishment, proliferation and spread (Carlton, 1996). Proliferation and spread each depend on reproduction, such that invasion success is strongly influenced by the production, dispersal and traits of propagules (Kinlan & Hastings, 2005). In addition to the size of reproductive events (propagule pressure; Lockwood et al., 2005), the timing of propagule release can influence the successful establishment of introduced species (Johnstone, 1986). Given the role of early life history stages in dictating survival through to reproduction, there can be strong selection to optimize the timing of reproductive events and early development (Lee, 2002). Indeed, strong seasonal trends in the reproduction and early development of many invasive species are

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Author's personal copy Hydrobiologia

apparent, which in some instances differ between introduced and native ranges (e.g. Shenkar & Loya, 2008; Hierro et al., 2009). This may occur in response to altered abiotic conditions or to an assemblage of predators or competitors that differ in phenology to those in the invader’s native range (Breen & Metaxas, 2009). For example, whereas native populations of the ascidian Herdmania momus Savigny 1816 display year-round reproduction in the Red Sea, invasive populations in the Mediterranean have a short reproductive season, that is attributed to cooler winter temperatures and differential food availability (Shenkar & Loya, 2008). The European shore crab (Carcinus maenas, Linnaeus 1758), native to northwest Europe and North Africa (Broekhuysen, 1936; Naylor, 1962; Crothers, 1967), has established invasive populations on the Atlantic and Pacific coasts of North America, Japan, South America, South Africa and southern Australia (Carlton & Cohen, 2003; Thresher et al., 2003). Like many marine organisms, the crab has a planktonic larval stage, followed by a benthic juvenile phase. Although vectors such as ballast water have assisted in the translocation of C. maenas across the world, once established, C. maenas is able to extend its distribution through pelagic dispersal and adult migration (Thorson, 1961; Gomes, 1991; Queiroga, 1996, 1998; See & Feist, 2010). In both native and invasive populations of C. maenas, there is evidence that ovigerous females are present at multiple times of the year (e.g. Crothers, 1967; Queiroga, 1996; Yamada & Gillespie, 2008; Table 1). Carcinus maenas brood eggs for approximately 20 days (Berrill, 1982; Vinuesa, 2007). Adult populations may be estuarine or coastal, but larval development of each occurs at sea (Crothers, 1967). The ovigerous females of estuarine populations migrate towards the sea and larvae are hatched from eggs in the lower parts of estuaries during nocturnal ebbing tides (Queiroga et al., 1994). Larvae hatched within estuaries are typically transported to the sea shortly after spawning where they pass through four zoeal and a megalopal stage (Crothers, 1967). The total planktonic duration may range from 27 to 53 days, depending on temperature and salinity (Nagaraj, 1993). Megalopae may reinvade estuaries, or remain in the coastal environment, settle and metamorphose into benthic juveniles (Queiroga, 1996). The settlement of C. maenas represents an active

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response by the megalopae to the substrates they encounter (Moksnes et al., 2003). Successful settlement and, hence, recruitment (i.e. survival of newly settled individuals to measureable sizes) of C. maenas to benthic habitats is more temporally constrained than is the production of eggs (Table 1). Settlement primarily occurs in summer and autumn, although this is not the case in Portugal where recruitment occurs year-round (e.g. Crothers, 1967; Berrill, 1982; Baeta et al., 2005; Table 1). Within the native range of C. maenas, crab larvae start hatching when water temperatures exceed 10°C in salinities above 26% (Crothers, 1967). Throughout its distribution, temperature influences survival, growth and the food intake of C. maenas larvae, with larval development proceeding at temperatures of 12–25°C and time to settlement decreasing as temperature increases (Dawirs, 1985; Nagaraj, 1993; de Rivera et al., 2007). Temperature has been shown to be a good predictor of C. maenas presence around the globe and its potential to invade suitable habitats (Yamada & Kosro, 2009; Compton et al., 2010). Little is known about the timing of C. maenas reproduction and benthic recruitment in Australia, where the crab has been present since at least the late 1800s (Fulton & Grant, 1900). As compared to many European estuaries where water temperature falls below 10°C during winter, water temperatures of New South Wales (NSW) estuaries are much warmer, with the average temperature for winter typically ranging from 11.5 to 20°C in winter and 15.5 to 25°C in summer (Poore, 2004). Hence, the temperature required for reproduction of C. maenas may be met year-round, potentially enabling successful recruitment to the benthic juvenile stage in multiple seasons. Along the mainland coastline of Australia, C. maenas populations are small and highly ephemeral (Garside et al., 2014), making studying the species’ early life history difficult. A recent trapping study on the south coast of NSW yielded a catch per unit effort of only 0.06 adult crabs per trap (Garside et al., 2014). Difficulties in studying recruitment of the crab, caused by its low abundance, are compounded by a poor understanding of the key habitats into which the crab settles. Along the south-east Australian coast, the crab’s distribution overlaps with that of biogenic habitats, such as mangroves, that are not present elsewhere within the crab’s range (Garside & Bishop,

Wi–Sp Au–Sp Au–Sp

Nova Scotia, Canada

Northwest, North America

San Jorge Gulf, Argentina

Eden, New South Wales, Australia

7–16.8

8–23 Sp

Wi

Su 7–8.2

8–22

Wi

Su–Au

Su–Au 9–18

Au

Lab data from lab experiments only, Sp spring, Su summer, Au autumn, Wi winter

The temperature (Temp) at which each stage of development has been observed to occur at each location is also indicated

Su–Au

Prince Edward Island, Canada

16–23

9–15

All year

Wi

Sp

Season

Au

Sp–Su Su

Invasive range Central Maine, United States Su–Au

Su–Au

12.7–23.3

14.5

Temp °C

Settlement

Su–Au

16–23

11–17

Sp–Au

All year

Sp

Sp–Su

Su

Season

Megalopae found

Gullmar Fjord, Sweden

Helgoland, Germany

12.7–23.3

12.7–23.3

12.5–14.5 12–24

All year

All year

Wi–Sp

Temp °C

Mondego estuary, Portugal

12.5

All year

Sp–Su

Season

Au–Sp

Wi

Ria de Aveiro, northern Portugal

16–19 (lab)

Temp °C

Zoeae in Plankton

Ria Formosa lagoon, Portugal

Wi–Su Wi–Sp

Swansea, Wales

Sp–Su

Season

Ovigerous female

Milford Haven, Wales

Menai Strait, Wales

Native range

Place

Table 1 The timing of key events in the reproductive cycle of Carcinus maenas, in its native and invasive ranges

5–19

9.5

18

12–16

Temp °C

Pollard & Rankin (2003)

Vinuesa (2007)

Yamada & Gillespie (2008)

Cameron & Metaxas (2005)

Audet et al. (2008)

Berrill (1982)

Eriksson & Edlund (1977)

Dawirs (1985)

Baeta et al. (2005)

Sprung (2001)

Queiroga (1996)

Crothers (1966, 1967)

Naylor (1962)

Zeng & Naylor (1996)

References

Author's personal copy

Hydrobiologia

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2014). Consequently, key nursery habitats cannot necessarily be inferred from studies done elsewhere. Carcinus maenas primarily recruits to structurally complex habitats (Eriksson & Edlund, 1977; Sprung, 2001; Moksnes, 2002). Structured artificial collectors may provide a useful tool for the detection of the presence of megalopae in otherwise structureless habitat, or where there is a poor understanding of the key nursery habitats of the crab (Paula et al., 2006). In Portugal, plastic artificial turf has been successfully used as a recruitment substrate for C. maenas (Amaral & Paula, 2007). In east Australian estuaries, where C. maenas has been observed to recruit to bags of commercially cultured oysters (J. Mackay, pers comm), bags of live or oyster shells may also serve as a suitable unit with which to assess temporal patterns of recruitment. A novel detection experiment was designed to: (1) develop a method for detecting C. maenas recruitment to benthic habitats in south-east Australian estuaries; (2) assess the timing of C. maenas recruitment in a south-east Australian estuary; and (3) use the method to compare the timing of C. maenas recruitment with that of native crabs. We hypothesised that: (1) all crabs would recruit in greater numbers to structured than unstructured habitats; (2) C. maenas would recruit during the Austral autumn and spring when temperatures are similar to the time of year at which C. maenas recruit in their native range, and (3) the timing of C. maenas recruitment would differ to that of native crabs. Observations of recruitment of C. maenas to different substrates were coupled with a cohort analysis of C. maenas sampled in a nearby estuary, which provided additional information on the timing of recruitment.

1.5 m, between which trays of oyster bags could rest at a mid-intertidal elevation of Mean Low Water Springs ?1.0 m (Fig. 1). The lease was chosen for assessments of Carcinus maenas recruitment because: (1) recruits of this species have previously been observed at this site (J. Mackay, pers comm); (2) the lease was situated over a Posidonia australis Hooker, 1858 meadow, and in other parts of its range, C. maenas has been observed to settle in seagrass (Sprung, 2001; Moksnes et al., 2002); and (3) Merimbula Lake has been demonstrated to have a persistent population of C. maenas (Day & Hutchings, 1984; Glasby, unpubl data). During the study, the water temperature at the study site ranged from 10 to 26°C, and salinity ranged from 20 to 38% (NSW Food Authority, unpubl data). Tides were diurnal with an amplitude of *1.5 m in the lake. Four substrate treatments were used in the assessments of C. maenas and native crab recruitment: empty, plastic artificial turf, live oysters (a mix of S. glomerata and C. gigas) and oyster shells. It was hypothesised that crabs would recruit in greater numbers to the three structured treatments than to the empty treatment, and that among the structured treatments, crabs would recruit in greater numbers to live oysters than to oyster shells, and oyster shells than to turf. Live oysters represent a potential food source to the crabs (Mascaro´ & Seed, 2001), and oysters, which were of variable size (see below), provided a habitat of greater heterogeneity (number of different structural elements; McCoy & Bell, 1991) than the turf.

Materials and methods Merimbula Lake recruitment study Assessments of crab recruitment and growth were done in Merimbula Lake, on the south coast of New South Wales (NSW) Australia (36.89oS, 149.92oE), on an oyster lease in which native Sydney rock oysters (Saccostera glomerata: Gould, 1850) are cultivated and non-native Pacific oysters (Crassostrea gigas; Thunberg, 1793) also colonise the leases. The lease consisted of parallel wooden rails, separated by

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Fig. 1 Live oyster, oyster shell, turf and bare treatments were enclosed within 3-mm mesh oyster bags, which were deployed on intertidal trays of a Merimbula Lake oyster lease. Each tray held up to three bags


Each treatment was enclosed within 445 9 850 9 90 mm mesh bags, constructed of 3 mm mesh non-toxic UV stabilised plastic mesh (Zapco Aquaculture Ltd.). This mesh size was sufficiently large that C. maenas megalopae could settle inside the mesh bags, but sufficiently small that following minimal growth the crabs were unable to escape. The bags and turf were weathered outdoors for at least 1 week prior to their initial deployment. The bags assigned to the empty treatment did not receive any substrate. The bags assigned to the artificial turf treatment received a 400 9 500 mm piece of green polyethylene Kindy Turf, of 19 mm thickness (Synthetic grass & rubber surfaces, Australia Pty Ltd). This treatment was included because a study by Amaral & Paula (2007) found that artificial habitat was just as efficient as natural substrates in collecting C. maenas in its native range. Bags assigned to the live oyster treatment received a *50:50 mix of native Sydney rock oysters (S. glomerata) and non-native Pacific oysters (C. gigas). These oysters were sourced from the Merimbula Lake oyster lease (where S. glomerata were farmed and C. gigas were present as overcatch), and provided a heterogeneous substrate due to differing shell morphologies and because C. gigas are typically larger (Krassoi et al., 2008). On average, at the start of the experiment, there were 3300 oysters of 3–8 mm shell height, 477 of the 12 mm oysters, 250 of the 16 mm oysters, 67 of the 20 mm oysters and 10 oysters that were [20 mm in shell height. As the oysters grew, their number was reduced to maintain a volume of 5 L per bag. The oyster shell treatment received 5 L of oyster shell per bag, of a similar size and species distribution to the live oyster treatment. To assess the timing of C. maenas and native crab recruitment, 10 bags of each treatment were deployed quarterly, from September 2011 to October 2013. Bags were deployed in random order on 2500 9 1000 9 40 mm oyster trays, with up to three bags per tray (Fig. 1). Each set of bags was left in the field for 3 months. Hence, recruitment was assessed twice, over a 24-mo period, in each of: (1) spring (September–November); (2) summer (December–February); (3) autumn (March–May); and (4) winter (June–August). At the end of each deployment period, bags were removed from the oyster lease and the contents of each washed separately through a 10-mm screen onto a

1-mm sieve within 4 h of collection. Material retained on the 10-mm screen was also visually checked for crabs and if found, they were added to the contents of the 1-mm sieve. Material retained on the 1 mm sieve was transferred to a container and immediately frozen. In the laboratory, samples were thawed and benthic phase crabs were separated from small shell fragments and organic material under a lamp. Under a dissecting microscope the crabs were then identified (according to Poore, 2004), enumerated by species, and sized by measuring the carapace width at its widest point (between anterolateral spines for species where they were present) to the nearest 0.1 mm, using digital callipers. PERMANOVA (Anderson et al., 2008) was used to test the hypothesis that the abundance of C. maenas recruits, and the most abundant native crab recruits would vary among substrates and seasons. The analyses had three factors: (1) treatment (4 levels: live oyster, dead oyster shell, artificial turf, empty); (2) season (4 levels: summer, autumn, winter, spring); and (3) year (2 levels: year 1, year 2), with n = 10 bags per treatment. Where significant effects were seen (at a = 0.05), the PERMANOVA analyses were followed by pair-wise post hoc tests to assess differences between levels of treatments. Fisheries Creek cohort analysis To assess whether the times of year at which C. maenas recruits was similar in a second NSW estuary, we opportunistically used data collected by the Sapphire Coast Marine Discovery Centre from a trapping survey in Fisheries Creek, to conduct a cohort analysis. Fisheries Creek is a small intermittently closed lagoon 23 km south of Merimbula Lake, on the southern side of Twofold Bay, NSW (37.11oS, 149.92oE). Fisheries Creek contains among the highest abundances of C. maenas in NSW (Pollard & Rankin, 2003). Trapping in Fisheries Creek was carried out on 20 sampling dates between February 2007 and November 2010. Although the timing of this sampling differed to that of the recruitment study, our goal was to assess whether there are certain times of year at which new recruits are apparent that are consistent among years. On each occasion, 10–12 ‘Opera House’ fish traps (640 9 460 9 210 mm), constructed of green 10 mm mesh with an 85 mm diameter hard circular opening at

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Author's personal copy Hydrobiologia 8.0

a Live

6.0

Shell Turf

4.0

Empty (no substrate) 2.0 0.0

Abundance (no. per bag)

either end were deployed at least 10 m apart. These traps were effective at capturing and retaining crabs [20 mm in carapace width, with crabs in the 16–20 mm size class and smaller likely underrepresented (pers obs). Each trap was baited with an 8–15 cm pilchard (Sardinops neopilchardus) and left to fish for 22–24 h. Traps were either set near the mouth of the estuary on sand or further up the creek on muddy sand in water \1 m depth. At the end of each deployment period, the number of crabs caught by each trap was counted, crabs were sized to the nearest mm using the method described above, and the number of females that were gravid was recorded. Using these data, we constructed size frequency histograms for each sampling time, standardised to trapping effort (i.e. average number per size class per trap). Standardisation was necessary due to the variable number of traps set on each date. Using the size frequency histograms, we identified months in which new cohorts (i.e. individuals smaller than those detected on the previous date of sampling) were apparent for the first time.

8.0

b 6.0 4.0 2.0 0.0 8.0

c

6.0 4.0 2.0 0.0

Results

Sp

Su

Au

Year 1

Wi

Sp

Season

Su

Au

Wi

Year 2

Merimbula Lake recruitment study Among the bags deployed for 3 months, the abundance of Carcinus maenas differed according to the three way interaction between Treatment 9 Season 9 Year (PERMANOVA: Pseudo-F(9288) = 15.84, P = 0.001; Fig. 2). In winter of Year 2, significantly more C. maenas were detected in bags of live oysters than in the other three treatments (post hoc tests, P \ 0.05; Fig. 2). At all other times (when abundances of recruits were low) there was no significant difference among the four treatments (post hoc tests, P [ 0.05, Fig. 2). No crabs were observed in the empty bags at any of the sampling times. No significant difference among seasons was found for any of the other treatments, in year 1 or year 2, or for the live oysters in year 1 (post hoc tests, P [ 0.05; Fig. 2). Across all treatments, observations of C. maenas were confined to spring of Year 1, and spring and winter of Year 2. In addition to C. maenas, 13 species of native crab were collected in bags during our study (Table 2). Among these, Pilumnopeus serratifrons Kinahan 1856 (Smooth-Handed Crab) and Halicarcinus ovatus

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Fig. 2 Mean (?SE) abundance per bag of a Carcinus maenas, b Pilumnopeus serratifrons, and c Halicarcinus ovatus at the end of each 3-mo deployment period. Sp spring, Su summer, Au autumn, Wi winter. Year 1 = September 2011–August 2012; Year 2 = September 2012–October 2013. n = 10

Stimpson 1858 (False Spider Crab) were the most abundant, accounting for 55 and 21% of all crabs, respectively (Fig. 2). Of the 13 native species, six recruited only in autumn, one recruited only in summer, two recruited in late summer and early autumn, one recruited only in winter one recruited in late winter and spring, while the other two recruited year-round (Table 2). The number of P. serratifrons that recruited to bags varied according to the three way interaction between Treatment 9 Season 9 Year (PERMANOVA: Pseudo-F(9288) = 5.85, P = 0.001; Fig. 2). In year 1, the abundance of P. serratifrons in bags with structured habitat (i.e. live oyster, dead oyster, or turf) was greater in autumn than at the other three times of year (post hoc tests, P \ 0.05; Fig. 2). In the empty

Author's personal copy Hydrobiologia Table 2 The total number, by species, of crabs detected in bags deployed for multiple 3-mo periods (over 2 years), their mean (±SE) and range in carapace width (mm) and their season of recruitment to the bags

Species Carcinus maenas Pilumnopeus serratifrons

a

Found in first year

b

Found in second year

Mean size (mm)

Range (mm)

Season found

30

6.7 (1.3)

2.5–14.1

Spa,b, Wia

254

4.9 (0.4)

1.9–15.1

All

Halicarcinus ovatus

96

5.0 (0.3)

1.4–7.7

All

Litocheira bispinosa

41

3.0 (0.1)

1.5–5.2

Spa, Wia

Brachynotus spinosus

8

9.3 (0.1)

9.0–10.2

Sua,b, Aua

Amarinus lacustris

8

3.5 (0.1)

2.7–4.7

Sua,b

Paragrapsus laevis

6

7.5 (0.5)

3.7–11.1

Sua, Aua

Thalamita sima Notomithrax minor

2 1

5.4 (0.2) 5.8

4.5–6.2 5.8

Aua Aua

10

3.3 (0.1)

2.5–3.8

Aua,b

Ocypode convexa

3

5.9 (0.3)

4.7–6.2

Aub

Macrophthalamus crassipes

5

4.4 (0.3)

3.4–5.4

Aua

Parasesarma erythrodactyla

1

2.5

2.5

Wia

Charybdis orientalis

1

8.7

8.7

Aua

Ilygrapsus paludicola Sp spring, Su summer, Au autumn, Wi winter

Total

bags, in which there were fewer of this crab, there was no significant difference in abundance among seasons (post hoc tests, P [ 0.05). In year 2, the abundance of P. serratifrons was greater in autumn than winter among the bags with live oysters or shell and greater in autumn than in spring or summer among bags with shell or turf treatment (post hoc tests, P \ 0.05; Fig. 2). The abundance of H. ovatus recruits in bags varied according to Treatment (PERMANOVA: PseudoF(3288) = 3.51, P = 0.017; Fig. 2) and Year (PERMANOVA: Pseudo-F(1288) = 10.19, P = 0.004; Fig. 2), but displayed no significant interaction among factors or a main effect of Season (PERMANOVA, P [ 0.05). Pair-wise tests showed no difference in abundance for H. ovatus among the structured treatments (post hoc tests, P [ 0.05), but indicated significantly more H. ovatus in the bags of structured habitat than in the empty treatment (post hoc tests, P \ 0.05; Fig. 2). Halicarcinus ovatus was significantly more abundant in Year 1, than Year 2 (post hoc tests, P \ 0.05; Fig. 2). Fisheries Creek cohort analysis Over our 45-mo study of the Fisheries Creek C. maenas population, we detected five main periods in which crabs [16 mm recruited (Fig. 3), namely (1) prior to February 2007; (2) between November 2007 and March 2008; (3) between December 2008 and

February 2009; (4) September 2009; and (5) between December 2009 and March 2010. In addition to these main recruitment events, small numbers of crabs of the smallest detectable size class were detected in March and May 2010. Gravid females were found on six occasions over the three-year period, between May and November (Table 3). Over these six occasions, the percentage of females that were gravid ranged from 4 to 19% (Table 3).

Discussion In combination, our recruitment study and cohort analysis indicated that in south-eastern Australia, C. maenas megalopae primarily settle in the late Austral winter to spring. By contrast, crabs native to southeastern Australia primarily recruited in autumn (Table 2). Hence, based on the results of this study, the timing of peak C. maenas recruitment in south-eastern Australia appears to differ from high latitude locations in the crab’s native and invasive range where recruitment primarily occurs in autumn (e.g. Berrill, 1982; Audet et al., 2008; Table 2). This disparity likely reflects the warmer water temperatures within southern NSW, but this timing of recruitment may also modify interactions between C. maenas and native Australian crabs. Quarterly deployments of natural and artificial substrate to Merimbula Lake over 2 years revealed

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Fig. 3 The size distribution of Carcinus maenas trapped within Fisheries Creek, NSW, on 20 samling dates between February 2007 and November 2010. The five main recruitment events

detected by our traps are shown in grey. Size distributions are expressed as Catch Per Unit Effort (CPUE; the number of traps deployed). n = 1391 crabs detected across the 20 trapping dates

that in each year, C. maenas recruitment peaked in late winter or early spring. The cohort analysis, conducted on data acquired from a nearby lagoon, Fisheries Creek in Twofold Bay, over nearly 4 years, revealed that the smallest size class of C. maenas trapped

(16–20 mm) was sampled primarily in summer (four of the five occasions). Based on the observation that juvenile C. maenas were 2.5–14.1 mm in recruitment bags deployed for 3 months during our south-east Australian study (Table 2), 14 mm in carapace width

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Author's personal copy Hydrobiologia Table 3 Sampling times at which the numbers of males were caught, gravid females were detected in Fisheries Creek, and their percentage contribution to the total females caught

Month

Year

Total males caught

Total females caught

February

2007

79

61

0

April

2007

26

93

0

May July

2007 2007

50 21

65 26

18 19

September

2007

5

2

0

November

2007

4

12

8

March

2008

14

24

0

April

2008

13

29

0

December

2008

3

0

0

February

2009

29

28

0

June

2009

69

61

5

August

2009

23

47

4

September

2009

33

26

15

October

2009

11

13

0

November

2009

18

67

0

December

2009

10

11

0

March

2010

23

29

0

May

2010

5

4

0

October November

2010 2010

12 13

4 13

0 0

2–6 months after settlement in the Pacific northwest (Yamada et al., 2005), 7–13 mm by 3–4 months after settlement in Denmark (Rasmussen, 1973), and 5–20 mm by 3–6 months after settlement in Sweden (Moksnes, 1999), it seems that recruits of 16–20 mm would be 3–6 mo old and so derived from a late winter or spring settlement event. Hence, in south-eastern Australia the reproductive phenology of C. maenas may more closely match that displayed by the crab in Portugal, where settlement, although occurring yearround (Baeta et al., 2005), tends to peak in winter and spring (Queiroga, 1996; Sprung, 2001), than that at higher latitudes (mainly autumn settlement; Table 1). Although in Merimbula Lake we detected recruitment of C. maenas only in late winter and early spring, ovigerous females were detected in nearby Fisheries Creek, from May to November and in previous studies in south-eastern Australia between April and November (Glasby, unpubl data; Pollard & Rankin, 2003). If C. maenas brood eggs for approximately 20 days (Berrill, 1982; Vinuesa, 2007), eggs may be released from June to December resulting in settlement from July to January (winter–spring) if the planktonic duration is 25 days (at 20°C) to 40 days (at 15°C;

Percentage of females that were gravid (%)

Nagaraj, 1993). A broader settlement period was supported by the trapping in Fisheries Creek which primarily detected recruits of a size consistent with spring settlement. However, on several occasions in Fisheries Creek small numbers of crabs were caught that appeared to have come from settlement events at other times of the year. Hence, it seems that a broad window of settlement may be possible in south-eastern Australia (perhaps only under specific environmental conditions); however, settlement peaks in late winter to early spring, perhaps due to pre-settlement mortality reducing the survival of larvae and megalopae through to settlement at other times of the year. The failure of our recruitment bags, deployed in Merimbula Lake, to detect recruitment outside of the peak event may have been a consequence of limited spatial replication. Studies done elsewhere within the native and introduced ranges of C. maenas suggest that at high latitude locations, warming of waters following winter triggers reproduction of C. maenas (Crothers, 1967; Audet et al., 2008; Table 1). In Portugal and Australia, however, the low temperatures of less than 10°C which prevent the hatching of eggs (Crothers, 1967) and of less than 12°C that stall larval development

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(de Rivera et al., 2007) rarely occur. In Merimbula Lake, where our recruitment study was done, the average minimum sea temperature in the coolest months of July and August is 14.9°C and the lowest water temperature that we have recorded in the estuary is 9°C (C.J. Garside, unpubl data). Peak summer water temperatures may, instead, limit larval survival. Sprung (2001) found C. maenas larvae were present only at temperatures below 23°C. Ovigerous females were notably absent from Merimbula Lake in the warmest month (March), when the average maximum sea surface temperature was 23.8°C. In south-eastern Australia late winter to early spring recruitment does, however, overlap with peaks in rainfall and river flow that may reduce salinities below those suitable for larvae and newly settled juveniles. In displaying a recruitment peak that differs in timing to many crabs native to south-eastern Australia, C. maenas may be able to minimise interactions with potential competitors. Of the thirteen species of native crab detected by this study, eleven displayed peak recruitment periods outside of the period of C. maenas recruitment for the substrates examined here. This included the most abundant taxon of native crab at our study site, Pilumnopeus serratifrons, which accounted for over 50% of total crabs. Only three species of native crab were found to have temporal windows of recruitment that overlapped with the late winter– spring recruitment peak of C. maenas: P. serratifrons, which displayed some minimal recruitment yearround; Halicarcinus ovatus, which also recruited year-round; and Litocheira bispinosa Kinahan 1856, which although displaying a very similar pattern of recruitment to C. maenas, accounted for less than 10% of the native crabs recruiting to our bags (Table 2). The two most abundant species of native crab at our site, P. serratifrons and H. ovatus, are each scavengers and micropredators on invertebrate prey (Taylor & Poore, 2011a, b). Hence, at high densities they may compete for food with the omnivorous C. maenas (Ropes, 1968). By minimising overlap in recruitment with these two species, C. maenas may reduce competition for food resources. If, however, food resources are depleted by crabs over time, the native species may be advantaged and C. maenas disadvantaged by the generally earlier recruitment of the native species. By recruiting at a different time of year to most native crabs, C. maenas may minimise physical interactions at small sizes when it cannot compete with native crabs.

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The settlement of C. maenas represents an active response by the megalopae to the substrates they encounter (Moksnes et al., 2003). Previous studies have found greater recruitment of C. maenas to structured than unstructured habitats (Moksnes, 2002). Greater recruitment to structured habitats may be driven by the strong selective pressure of reduced post-settlement mortality (Moksnes et al., 1998) or by a greater surface area for attachment of benthic invertebrate prey (Moksnes, 2002). Here, we observed recruitment to our bags with structural habitat but not those that were empty. Among bags with structural habitat, those with live oysters collectively contained the greatest overall number of C. maenas when summed across the study, but this pattern was driven by a difference among habitats at a single time point. Despite similar recruitment of C. maenas to artificial turf and natural substrates in previous studies (Amaral & Paula, 2007), the bags with artificial turf collected fewer crabs than the live oyster bags here. Although live oysters offered habitat of greater heterogeneity than the artificial turf mats, habitat heterogeneity alone could not explain differences in recruitment among substrates. The oyster shell offered a habitat that was just as heterogeneous, if not more so, than the live oysters, but overall supported fewer crabs. Complexity (the absolute number of individual components per unit area; McCoy & Bell, 1991) was greater for the turf than either of the oyster treatments. Instead, the potential for live oysters, but not oyster shell or turf, to serve as a food resource for C. maenas may, in part, explain the result. Oyster farmers have observed crushed oysters in bags into which C. maenas have settled, consistent with predation (J. Mackay, pers comm.). Our study suggests that trays of commercially cultivated oysters or specially deployed bags containing small oysters are likely to be appropriate for surveillance of C. maenas recruits along the New South Wales coastline. It also reinforces the view that translocation of cultured oysters may potentially be a mechanism of C. maenas spread in Australia (Thresher et al., 2003) and elsewhere (Yamada & Gillespie, 2008). Our results do not necessarily suggest that natural oyster reef is a key site for settlement because artificial collectors, such as ours, provide substrate for settlement in areas where megalopae may normally pass over benthic substrates (Paula et al., 2006). A survey of natural substrates


would be required to assess recruitment to natural habitats. Overall, recruitment of C. maenas to the experimental bags was low. This was expected given the extremely low abundance of adult C. maenas in east Australian estuaries (Garside et al., 2014). Nevertheless, it is possible that predation of early (larger) recruits on later (smaller) recruiting crabs led to early post-settlement mortality and hence reduced numbers of recruits (Moksnes, 2004). It is also possible that other substrates, not trialled by this study, may collect greater numbers of recruits. In summary, our study suggests that in southeastern Australia, C. maenas displays a much longer reproductive season than in higher latitude locations, resulting in a late winter–spring recruitment peak. Although likely reflecting a release from the water temperature constraints of cooler climates, this strategy has the potential to benefit C. maenas by minimising temporal overlap in recruitment with native crabs, potentially allowing pre-emption of resources such as food and space by the non-native crab. This strategy also allows temperature-sensitive stages in the reproductive cycle to occur outside of summer temperature extremes. In demonstrating that peak recruitment of C. maenas in eastern Australia occurs primarily in late winter–spring, and that oyster bags are successfully colonised, our study provides guidance to surveillance programmes aimed at early detection of the invader at new locations along the Australian coastline. Acknowledgments We thank the Sapphire Coast Marine Discovery Centre for providing the trapping data for Fisheries Creek. G. Meini, A. Gehin, J. Rowland, R. Furtado, J. Kenworthy, D. Bateman and S. Lamesa assisted with fieldwork. J. Mackay, C. and D. Boyton and S. Cullenward provided access to oyster leases and assisted with field logistics. S. Ahyong of the Australian Museum provided assistance with the identification of crabs. B. Kelaher, M. Coleman, D. Barneche, D. Johnson and anonymous reviewers provided helpful comments that improved the quality of the manuscript. This study was funded by an Australian Research Council (ARC) Linkage Grant to M. Bishop, M. Coleman, T. Glasby and B. Kelaher, with industry partners, the NSW Department of Primary Industries, Southern River Catchment Authority and Bateman’s Marine Park. This work was performed during a Ph.D. candidature at Macquarie University during which C. Garside was in receipt of an Australian Postgraduate Award Industry (APAI) and an International Macquarie Research Excellence Scholarship (IMQRES). Experiments performed in this study complied with the current laws for manipulative field experiments and capture of animals within Australia.

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