Freshwater Biology (2010) 55, 2011–2022 doi:10.1111/j.1365-2427.2010.02457.x

Reproductive traits of riverine shrimps may explain the impact of altered flow conditions

ADAM RICHARDSON* AND PAUL HUMPHRIES† *Murray-Darling Freshwater Research Centre, La Trobe University, Wodonga, , †Institute for Land, Water and Society, School of Environmental Sciences, Charles Sturt University, Albury, NSW, Australia

SUMMARY 1. The response of a species to environmental disturbance is largely mediated by its life history traits that have evolved within a particular habitat template. Altered flow seasonality, as a direct consequence of river regulation, is a major environmental disturbance and has been implicated in the redistribution of a range of riverine organisms. An understanding of the reasons for species-specific responses, however, has proved elusive. 2. Here, we investigated the reproduction of three riverine shrimp species ( australiensis, Caridina mccullochi and Macrobrachium australiense) that show contrasting patterns in distribution and abundance in regulated Australian rivers. 3. In all three species, breeding females were largest, and fecundity was greatest early in the breeding season (November–December). Fecundity and egg size subsequently declined, with lower investment (overall and per offspring) perhaps indicating that conditions for larvae were more favourable later in the breeding season (a time normally characterised by low flow, warm water and high productivity). 4. Interspecific differences in absolute values of reproductive traits were, however, striking. Paratya australiensis has typically ‘opportunistic’ traits (small body size, small eggs and high fecundity), whereas M. australiense has more ‘equilibrium’ traits (larger body size, larger eggs and moderate fecundity). Caridina mccullochi is intermediate, having neither high fecundity nor large size, and has limited swimming ability when young. This species is now absent from at least one heavily regulated river in south-eastern Australia, and we hypothesise that its life history may explain this absence. 5. Studies involving aspects of life history, such as reproductive traits, are likely to improve our understanding of a range of organisms and assist in the management of disturbed or altered environments.

Keywords: aseasonal flow, environmental disturbance, life history, lowland rivers, Murray–Darling Basin

that maximises fitness under a defined set of environ- Introduction mental conditions (Stearns, 1992). Although the envi- One guiding tenet of ecology is that life history traits of ronmental conditions under which a species can live organisms have evolved in the context of a habitat varies naturally at several temporal scales, anthropo- template (Southwood, 1977). Through the process of genically induced changes often alter conditions natural selection, a species’ suite of traits has evolved beyond tolerance limits. This can lead to a decline in diversity through a loss, or reduction in abundance, of Correspondence: Adam Richardson, Murray-Darling Freshwa- less tolerant species and an increasing dominance by ter Research Centre, La Trobe University, Wodonga, Victoria, opportunistic (often alien) species (Townsend & Hil- Australia. E-mail: [email protected] drew, 1994; Olden, Kennard & Pusey, 2008).

2010 Blackwell Publishing Ltd 2011 2012 A. Richardson and P. Humphries Life history theory provides some explanation for native fish while alien species increase (Gehrke et al., the responses of species to environmental disturbance 1995; Humphries et al., 2008). A recent study has also (Pianka, 1970; Stearns, 1976; Bongers, 1990; Taylor, suggested a link between changes to natural flow Aarssen & Loehle, 1990; Winemiller & Rose, 1992; patterns and the distributions of three caridean Lytle, 2001; Winemiller, 2005). ‘Opportunistic’ species shrimps (Richardson et al., 2004). Of particular inter- (sensu Winemiller & Rose, 1992; : with early maturity, est in this last study were species-specific abundance short life span, production of large numbers of small and distribution patterns in a heavily regulated river young – equivalent to r-selected species) should have with altered flow seasonality. In the Campaspe River, a relative advantage under disturbed, unpredictable P. australiensis (Kemp 1917) occurs in large numbers, conditions when mortality of young is high or whereas C. mccullochi (J Roux 1926) has apparently variable. ‘Equilibrium’ species (with later maturity, disappeared and production of M. australiense (Hol- larger and longer-lived than opportunistic species, thuis 1950) decreased in the most affected sections production of small numbers of large young – (Richardson et al., 2004). equivalent to K-selected species), on the other hand, The aim of this study was to investigate whether the are suited more to stable conditions, where food reproductive traits could explain the relative success resources and other factors related to survival of the of the three caridean shrimp species under altered young are more predictable. Some species may be flow conditions. Although reproductive traits, by intermediate and display traits of both r- and K- comparison with other aspects of life history, may selected species. Winemiller & Rose (1992) suggested have the greatest potential for predicting the impacts that these ‘periodic’ species are most suited to of anthropogenic disturbance (Resh et al., 1994; Gay- conditions that are relatively predictable over large raud et al., 2003), progress so far has been limited. spatiotemporal scales. This may be because of limited biological knowledge, Rivers represent some of the most heavily anthro- or because studied assemblages have been very pogenically modified environments on the planet. diverse (Resh et al., 1994; Gayraud et al., 2003; Diaz, Common modifications include alterations to Alonso & Gutie´rrez, 2008; Griswold et al., 2008; flow and thermal regimes, changes to longitudinal Tomanova, Moya & Oberdorff, 2008). Here, we and lateral connectivity, changes to the volume and describe the breeding period, size of berried females, arrangement of instream and riparian habitat fecundity, egg mass and reproductive output of and, consequently, changes in the distribution and three co-occurring caridean shrimps (P. australiensis, abundance of native flora and fauna (Petts, 1984; Bunn C. mccullochi and M. australiense) over the course of a & Arthrington, 2004). One of the more extreme breeding season (late spring to early autumn) in an modifications is the reversal of seasonal flow patterns, Australian lowland river. Specifically, we compared a common feature of rivers with headwater dams the reproductive traits among the three shrimp used mainly as reservoirs for irrigation purposes species and assessed whether interspecific differences (Petts, 1984). Under such conditions, high flows may can explain the species-specific responses to altered occur when flow is naturally low, as water is released flow seasonality observed previously (Richardson to supply downstream users. In contrast, water is et al., 2004). stored during natural high run-off periods for later release. The impacts of such modifications to natural seasonality are potentially severe, especially for non- Methods opportunistic species that have evolved under envi- Study area ronmental conditions that no longer exist (Winemiller, 2005). We collected shrimps from a 500 m reach of the Altered flow seasonality is one of the major effects Broken River (Scholes Road: 14556¢54¢¢E, 3630¢29¢¢S) of river regulation in the Murray–Darling Basin, in south-eastern Australia. This river was chosen as south-eastern Australia (Walker, 1992). Consequently, the study site for two major reasons: first, it is only a range of biological responses has been observed moderately impacted by flow regulation (only 10– such as the virtual extinction of some aquatic snails 20% of mean annual discharge is diverted for (Sheldon & Walker, 1997) and a reduced abundance of offstream use); and secondly, an earlier 3 year study

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 2011–2022 Reproductive traits of riverine shrimps 2013 found that the three species of shrimp occurred each Recent studies in inland Australian rivers (includ- year (16–38% P. australiensis, 37–53% C. mcculloch and ing the Broken River) have advanced considerably the 25–31% M. australiense; Richardson et al., 2004). understanding of riverine habitat use by each species (Richardson et al., 2004; Richardson & Cook, 2006; Price & Humphries, 2010): P. australiensis is a habitat Study species generalist with a preference for still and slow-flowing The atyid shrimps P. australiensis and C. mccullochi, water at all life stages; C. mccullochi has a strong and the palaemonid prawn M. australiense, are the preference for still and slow-flowing water, particu- only carideans found in the Murray–Darling Basin. larly at the larval and berried stages; whereas Considerable uncertainty exists regarding the taxo- M. australiense prefers still water as larvae, but the nomic status of P. australiensis and C. mccullochi. flowing main channel as berried and non-berried Currently, P. australiensis is considered to be a com- adults. Price & Humphries (2010) demonstrated that plex of cryptic species, and a number of divergent larvae of the atyids are retained in ‘slackwater’ habitat lineages may exist in the Broken River given that as patches until the final stage of development, but many as six are represented in the nearby Goulburn M. australiensis larvae mostly disperse from such River (Cook et al., 2006). We treat the complex in this areas as first stage larvae. In the Broken River and study as a single entity but recognise that there could nearby heavily regulated Campaspe River, larvae of be some variation in our results because of differences all species are most abundant between November and among lineages. We also treat C. mccullochi as a single March, and all species breed once annually in the entity, even though it has been described as species B Broken River, although P. australiensis probably within the Caridina indistincta complex Page, Choy & breeds again in the Campaspe River (Richardson Hughes (2005). In contrast, a low level of genetic et al., 2004). The shrimps in this study probably variation in M. australiense suggests that a single complete their life cycle in the Broken River and are species occurs throughout Australia (Murphy et al., unlikely to be amphidromous, as it is over 80 river- 2004). kilometres downstream to the Goulburn River and Both the and Palaemonidae are large, several thousand river-kilometres downstream to the diverse and ecologically important families (infraor- estuary (Richardson et al., 2004; Richardson & Cook, der ) occurring in tropical and subtropical 2006). Cook et al. (2006) acknowledged that, for regions throughout the world (Bauer, 2004). Although P. australiensis at least, there is an evolutionary tran- the Atyidae are predominantly a freshwater family, sition from amphidromous to freshwater life cycle. some species occur in saline waters during all life There are several other life history differences stages (Walsh & Mitchell, 1995), some have an among the three species. For example, larval devel- amphidromous life cycle and drift from freshwater opment varies considerably: eight stages lasting a into estuaries as larvae (March et al., 1998), and yet total of 28–45 days for P. australiensis (Walsh, 1993); others complete their entire life cycle in streams or seven stages over 20–25 days for C. mccullochi (Benzie, lakes (Fryer, 1977; Richardson et al., 2004). The pala- 1982) and three stages over only 6 days for M. aus- emonids occur across a similar range of freshwater traliense (Fielder, 1970). As adults, both of the atyids and saline environments (Magalha˜es & Walker, 1988). are of similar size. Paratya australiensis grows to about Of the study species, P. australiensis and M. austral- 40 mm total body length (Smith & Williams, 1980) iense are distributed widely throughout eastern Aus- and C. mccullochi is slightly smaller (A. Richardson, tralia (Cook et al., 2006; Murphy et al., 2004), but unpubl. data), and both have a life span of about C. mccullochi probably occurs only in some lowland 12 months (Richardson et al., 2004). Macrobrachium rivers of south-eastern Australia (see Richardson & australiense commonly grows to 65 mm and typically Cook, 2006). Paratya australiensis inhabits small upland lives for more than 2 years (Lee & Fielder, 1984). streams (Hancock & Bunn, 1997), turbid lowland rivers (Sheldon & Walker, 1997) and estuaries (Walsh Sampling, processing and data analyses & Mitchell, 1995), whilst M. australiense occurs in inland and coastal streams (Lee & Fielder, 1984) and Berried shrimp were collected each month between 21 lowland rivers (Sheldon & Walker, 1997). November 2002 and 12 March 2003 using a portable

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 2011–2022 2014 A. Richardson and P. Humphries backpack electrofisher (Smith-Root Model 12, http:// to compare CL, F, IEM and RO among ‘Species’ and www.smith-root.com) fitted with a 250-lm mesh net ‘Months’, with ‘Species’ and ‘Month’ considered fixed and removable collection jar (see King & Crook, 2002). factors. March was excluded from the analysis because We searched different habitats for berried specimens no berried female M. australiense were collected in that of each species (Richardson & Cook, 2006): still and month. Fecundity, IEM and RO were regressed against slow-flowing littoral areas for P. australiensis and CL to examine possible relationships between repro- C. mccullochi, and the faster flowing channel for ductive traits and shrimp size. Analysis of covariance M. australiense. Berried shrimps were immediately (ANCOVA) was conducted to compare the slopes of preserved in 70% ethanol, and all others returned linear relationships between pairs of shrimp species. alive to the river. All statistical analyses were carried out using SYSTAT Hydrological data were obtained from the Victoria 11 (SYSTAT Software Inc., Chicago, IL, U.S.A.) and Water Resource Data Warehouse (http://www. SPSS 14 (SPSS Inc., Chicago, IL, U.S.A.). vicwaterdata.net/), with discharge measurements taken from a gauging station at Casey Weir, appro- Results ximately 6 km downstream of the study reach. The water quality parameters temperature, conductivity, Hydrology and water quality pH, dissolved oxygen and turbidity were recorded Discharge at Scholes Road on the Broken River is with a Horiba U10 Water Checker (Horiba Ltd, Kyoto, typically strongly seasonal (Fig. 1). Based on a 30-year Japan) at Scholes Road in October and December mean, over 65% of the annual discharge (of about 2002 and February 2003 (see Humphries et al., 2008 2.2 · 108 m3) occurs in the 4-month period between for more details on antecedent conditions). July and October (winter ⁄spring) whereas, during the In the laboratory, a maximum of 10 berried females driest period (January–April), daily discharge is of each species were randomly selected from each ) <3.1 m3 s 1. The 10-year mean showed a substantial monthly sample. The carapace length (CL) of these fall in annual discharge (only 55% of 30-year mean), shrimps was measured to the nearest 0.01 mm. The due mostly to substantially reduced flows between entire brood of eggs was then removed from the July and October. Sampling was clearly undertaken pleopods with forceps and counted (F = fecundity). during a period of unusually low rainfall: in the Each brood was also staged according to egg eye period between April 2002 and March 2003, total development [as in Anger & Moreira, 1998: Stage I eye discharge was only 0.37 · 108 m3, daily discharge not visible; Stage II eye partially developed (small, ) varied between 1.01 and 1.59 m3 s 1, and the July– faint, linear or narrow); Stage III eye fully developed October period immediately prior to sampling (large and rounded)]. Egg stage was subsequently accounted for <25% of total annual discharge (Fig. 1). used as an approximation of breeding duration. In fact, discharge during the year that sampling was Reproductive output (RO) was calculated from the undertaken was outside the 95% confidence interval ratio of brood mass (BM) to shrimp mass (SM) and expressed as a percentage: RO=BM ⁄SM · 100 (Oh 25 et al., 2002; Anger & Moreira, 1998). Masses were

determined from dry weights and achieved, for each ) 20 –1

specimen, by drying separately to a constant mass, in s 30 year mean 3 an oven at 80 C for 24 h, the berried shrimps (minus 15 Sampling period eggs) and the corresponding brood and then weighing Nov 02 – Mar 03 10 10 year mean to the nearest 0.01 mg on an analytical balance. We

calculated the individual egg mass (IEM) by dividing Discharge (m 5 April 2002– the BM by fecundity: IEM = BM ⁄F. March 2003 0 Data were transformed, where necessary, to satisfy AMJASONDJFM J the requirements for normality and homeoscedasticity Month prior to performing ANOVAs, although results are Fig. 1 Mean daily discharge by month in the Broken River over presented as untransformed values in graphs for ease 30-year period with 95% confidence interval (dotted lines), of interpretation. Two-way ANOVAs were conducted 10-year period and 1 year including study period (shaded area).

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 2011–2022 Reproductive traits of riverine shrimps 2015 of the 30-year mean from June to December, and (a) Paratya australiensis January and February discharge was only just inside 100 the 95% confidence interval. 80 During the study period, there was only minor 60 variation in water quality parameters. Conductivity ) ranged from 138 to 162 lScm 1 (mean of 153 ± 5 (SE) 40 ) lScm 1), mean pH was 7.8 ± 0.1 (range 7.4 and 8.1), 20 )1 dissolved oxygen varied between 5.1 and 7.7 mg L 0 ) (mean of 6.1 ± 0.5 mg L 1) and turbidity ranged from 32 to 44 NTU (mean of 35 ± 2 NTU). Water temper- (b) Caridina mccullochi (n = 3) 100 ature ranged between 15.1 and 27.0 C, both values occurring in December. Average daily temperatures 80 were least early (November mean of 20.7 ± 0.30) and 60 late (March mean of 20.0 ± 0.24) in the season, and 40 highest in January (23.9 ± 0.21) and February 20 (23.7 ± 0.25). Composition (%) 0

Breeding periods (c) Macrobrachium australiense 100 An earlier study indicated that shrimp breeding in the Stage III 80 Broken River occurs predominantly between Novem- Stage II ber and March each year (Richardson et al., 2004). In 60 Stage I this study, Stage III eggs occurred on 30% of berried 40

P. australiensis in November, indicating that breeding 20 may have commenced earlier (Fig. 2a). Only 20% of 0 berried P. australiensis carried Stage I eggs in March NOV DEC JAN FEB MAR (down from a peak of 60% in January) suggesting that Month breeding beyond the study period was minimal. Stage III eggs were present on 20% of berried C. mccullochi Fig. 2 Percentage composition by month of development stages I, II and III of eggs carried by berried females of the three species in November, indicating that some breeding may during the breeding season. Eggs were staged from 10 shrimps have occurred prior to the study (the earlier study of each species each month (except for Caridina mccullochi in found that they rarely bred in October), but only Stage March, when only three berried individuals were collected). III eggs occurred in March, indicating that breeding ceased during that month (Fig. 2b). The entire breed- 339 eggs (range: 148–714), C. mccullochi 65 eggs ing period for M. australiense may have been captured (range: 24–90) and M. australiense 271 eggs (range: in this study, as only Stage I (50%) and Stage II (50%) 87–443) per berried female (Table 1); these differences eggs occurred in November, and there were no being significant among species (Table 2). Paratya berried females in March (Fig. 2c). australiensis eggs weighed, on average, just over 20 lg, <33% of the mass of a C. mccullochi egg and <10% of an average M. australiense egg (Table 1); Reproductive traits these differences among species being significant Although P. australiensis and C. mccullochi were sim- (Table 2). Overall reproductive output, however, ilar in size (mean CLs 5.38 and 4.58 mm, respectively) was similar among species: about 20% for P. austral- and M. australiense was much larger than either (mean iensis,22% for C. mccullochi and 21% for M. austral- CL of 12.33 mm; Table 1), the two-way ANOVA iense (Tables 1 & 2). indicated that all species were significantly different Carapace length, fecundity, IEM and reproductive from each other (Table 2; Tukey tests between each output all differed significantly by month, but none pair P < 0.001). Over their entire respective breeding of the interaction terms was significant (Table 2; periods, berried P. australiensis carried, on average, Fig. 3). Carapace length generally declined over the

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 2011–2022 2016 A. Richardson and P. Humphries

Table 1 Mean ± 1 SE carapace length, P. australiensis C. mccullochi M. australiense fecundity, individual egg mass and reproductive output of Paratya australien- Carapace length (mm) 5.38 ± 0.08 4.58 ± 0.06 12.33 ± 0.18 sis (n = 50), Caridina mccullochi (n = 43) Fecundity 339.12 ± 16.27 64.67 ± 2.83 271.25 ± 10.95 and Macrobrachium australiense (n = 40) for Individual egg mass (lg) 20.81 ± 0.88 70.57 ± 1.43 217.54 ± 3.67 the studied breeding season (November Reproductive output (%) 19.90 ± 1.04 22.29 ± 1.16 20.87 ± 1.08 2002–March 2003)

Table 2 F statistic and significance levels Carapace Individual Reproductive for two-way ANOVAs, with species and Source d.f. length Fecundity egg mass output month as factors, for Paratya australiensis, Caridina mccullochi and Macrobrachium Species 2 1629.9*** 453.3*** 3106.8*** 1.58 australiense from November 2002 to Month 3 7.7*** 15.1*** 5.9** 7.87*** February 2003 Species · Month 6 1.8 1.7 1.1 1.66 Error (MS) 108 0.007 0.014 0.003 0.019

**P < 0.01, ***P < 0.001. respective breeding periods (Fig. 3a), as did fecundity, production of relatively large eggs (possibly because with the number of eggs per female decreasing by only 20% of eggs were Stage I). For all species, 35% for P. australiensis,16% for M. australiense and reproductive output increased between November 44% for C. mccullochi (Fig. 3b). Individual egg mass and January before falling substantially, particularly also varied significantly among months, with larger for P. australiense and C. mccullochi (c.10%), in Feb- eggs produced between November and January (par- ruary (Fig. 3d). ticularly January) and smaller eggs from February (Fig. 3c). This pattern was somewhat obscured for Size relationships with reproductive traits M. australiense by the production of relatively small eggs in November (possibly because 60% of eggs Fecundity was significantly positively and linearly were Stage I), and for P. australiensis in March by the related to CL for P. australiensis (R2 = 0.62, P < 0.001,

16 250 (a) (c) 14

g) 200 m) 12 Paratya 10 150 Caridina 8 Macrobrachium egg mass (µ ce length (mm 6 100

4

Carapac 50

2 Individual

0 0

500 30 (b) (d) 25 400

20 300 15 er of eggs 200 Fig. 3 Monthly mean (± SE) (a) carapace 10 length, (b) fecundity, (c) individual egg Numb 100 mass and (d) reproductive output of the

Reproductive output (%) 5 three shrimp species collected during the

0 0 breeding season. For each species and NOV DEC JAN FEB MAR NOV DEC JAN FEB MAR each month n = 10, except for Caridina Month Month mccullochi in March (n = 3).

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 2011–2022 Reproductive traits of riverine shrimps 2017 overall mean ± 1 SE = 339.12 ± 115.07, n = 50), for C. mccullochi (R2 = 0.26, P < 0.001) (Fig. 4b). There C. mccullochi (R2 = 0.48, P < 0.001, mean ± 1 SE = was no significant relationship between CL and 64.67 ± 18.59, n = 43) and M. australiense (R2 = 0.28, reproductive output for P. australiensis, but there P < 0.001, mean ± 1 SE = 271.25 ± 69.25, n = 40) was a significant positive relationship for C. mccullochi (Fig. 4a). The slope of the line relating fecundity to (R2 = 0.11, P < 0.05) and a significant negative rela- CL was approximately five times steeper for P. aus- tionship for M. australiense (R2 = 0.13, P < 0.05), traliensis than for the other two species, and the although the amount of variation explained was relationship was significantly different between relatively small in each case (Fig. 4c). P. australiensis and C. mccullochi (ANCOVA, F = 116.67, P < 0.001) and between P. australiensis and M. australiense (ANCOVA, F = 48.317, P < 0.001), Discussion but not between C. mccullochi and M. australiense Environmental variables and the shrimp breeding season (ANCOVA, F = 0.874, P > 0.05). There was no significant relationship between The 2002–2003 shrimp breeding season was typical of CL and IEM for P. australiensis or M. australiense recent breeding seasons in the mildly regulated (P > 0.05), although there was a positive relationship Broken River. Water quality parameters (conductivity, pH, dissolved oxygen, turbidity and water tempera- ture) were all within the ranges and similar to the

800 averages recorded for that river (and studied reach) in (a) 700 y = 162.23x – 533.18 studies conducted since 1995 (Humphries, Serafini & 600 R2 = 0.6254 King, 2002; Richardson et al., 2004). This study, how- 500 y = 31.689x – 119.49 ever, clearly coincided with a prolonged period of low 400 R2 = 0.278 300 flow in the Broken River. The winter and spring 200 months prior to the study were characterised by very Number of eggs y = 34.667x – 94.269 100 R2 = 0.481 low flow, such that the hydrograph for the year that 0 included the study period (April 2002–March 2003:

300 study period November 2002–March 2003) varied (b) little seasonally, and only between January and March 250 did flows approximate the long-term average. Despite 200 this, the timing and duration of shrimp breeding in 150 y = 12.949x + 11.202 R2 = 0.2637 this study was consistent with previous shrimp 100 Paratya Caridina breeding seasons in the Broken River (Richardson 50 Macrobrachium et al., 2004); that is, P. australiensis had the longest Individual egg mass (µg) 0 breeding period and M. australiense had the shortest breeding period. 60 (c) 50 y = 6.8712x – 9.2099 Patterns in reproductive traits during the breeding 40 R2 = 0.113 y = –2.1566x + 47.459 R2 = 0.1316 season 30

20 The reproductive traits of the three shrimp species

10 followed similar patterns during the breeding season. Reproductive output (%) 0 For each species, breeding females were generally 2 4 6 8 10 12 14 16 largest early in the season (November–December) Carapace length (mm) and, consequently, fecundity was greatest at this time. Fig. 4 Regressions of (a) fecundity, (b) individual egg mass and The reduction in fecundity as the breeding season (c) reproductive output with carapace length for all berried progressed was accompanied by a reduction in the Paratya australiensis (n = 50), Caridina mccullochi (n = 43) and amount of reproductive investment per offspring. The Macrobrachium australiense (n = 40) collected between November 2002 and February 2003 from the Broken River. Linear equations size of caridean shrimp eggs is thought to be related to and R2 values given for significant relationships only. the environmental conditions awaiting newly hatched

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 2011–2022 2018 A. Richardson and P. Humphries larvae (Mashiko, 1990; Hancock, Hughes & Bunn, the Broken River, which provides the opportunity to 1998) – conditions considered short-term, localised construct hypotheses regarding shrimp responses to and variable from year to year (Clarke, 1993). Slower altered flow regimes. Indeed, the ranges of fecundities flow, higher water temperature and a greater abun- in this study were comparable with previously dance of food have been implicated in the production reported fecundities – P. australiensis (48–714 com- of smaller eggs (Mashiko, 1990; Clarke, 1993; Hancock pared with 29–1167 throughout its entire distribution: et al., 1998). This might suggest that conditions for Williams & Smith, 1979) without taking into account larvae in the Broken River improved as the season the complex of cryptic species (Cook et al., 2006); progressed, which is consistent with the observed C. mccullochi (24–90 compared with 50–100 in 24 river increase in water temperature and decrease in flow basins: Page et al., 2005); M. australiense (87–443 com- rate. pared with 61–473 in a river: Lee & Overall reproductive investment was greatest in Fielder, 1982). The interspecific differences in fecun- December and January for all species. Environmental dity and egg size in the Broken River were substantial conditions experienced by the female are thought to and statistically significant, such that comparisons be a major determinant of overall reproductive among species without potential trait profiles are investment (Mashiko, 1990; Hancock et al., 1998), reasonable. and the coincidence of high investment with favour- A plot of CL, fecundity and IEM indicates that able conditions can be considered an adaptation based P. australiensis has typically opportunistic traits, largely on long-term patterns, (Clarke, 1993; Hancock M. australiense more equilibrium traits, and C. mccullo- et al., 1998), such as the natural flow regime (Bunn & chi lies between the other two species (Fig. 5). Life Arthrington, 2004). In this study, therefore, there is a history theory suggests that the reproductive traits close match between the timing of favourable (if not associated with P. australiensis will provide a com- optimal) conditions for female shrimp (December– parative advantage under disturbed, unpredictable January) and larvae (February). The December to conditions (Winemiller & Rose, 1992; Winemiller, February period in the Broken River is typically a 2005), conditions like those we have described for period of low flow declining to very low flow. These the regulated rivers in the Murray–Darling Basin, and warm (summer), productive and stable conditions are ideal for the young of fish (Humphries et al., 2002; King, 2004) and, presumably, also for larval and juvenile shrimp.

Reproductive traits of shrimp species and impacts of altered flow regimes

Because of the similarities in seasonal trends in reproductive traits among the three shrimp species, interspecific differences in overall reproductive traits may instead provide better explanations for the apparent responses to altered flow regimes observed in an earlier study (Richardson et al., 2004). It must be recognised, however, that despite their having con- trasting life histories our study involves only three species, and so conclusions that we can draw are necessarily limited. Furthermore, describing the reproductive traits of shrimps throughout the species’ distributions would have permitted the development Fig. 5 Three-dimensional plot of logn transformed individual egg mass (IEW), fecundity (F) and carapace length (CL), and of more complete trait profiles, not to mention norms approximate position of opportunistic (O), equilibrium (E) and of reaction to different altered flow scenarios. How- periodic (Pe) life history strategies for Paratya australiensis (P), ever, considerable variation in traits was observed in Caridina mccullochi (C) and Macrobrachium australiense (M).

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 2011–2022 Reproductive traits of riverine shrimps 2019 the Campaspe River in particular (Richardson et al., usually declines during summer and, in the past, 2004). Paratya australiensis matures at a relatively small many rivers in this region would cease to flow entirely size, produces large numbers of relatively small by late summer. These warm, productive, stable young that probably experience high mortality at conditions are, presumably, ideal for young shrimps times during the breeding season when conditions (Richardson et al., 2004) and are likely to be the are not favourable. Aquatic macroinvertebrates with template on which their life history traits evolved more opportunistic (or r-selected) reproductive (Bunn & Arthrington, 2004). Following flow reversal traits typically dominate in disturbed environments and more constant high flow and typically cooler (Gayraud et al., 2003; Diaz et al., 2008; Griswold et al., water, still or slow-flowing rearing habitats are fewer, 2008). available food is affected (Humphries et al., 2002, By contrast, M. australiense has reproductive traits 2006), and we hypothesise that growth rates and more characteristic of equilibrium strategists, and, survival of young shrimp may diminish as a result. combined with its relatively short breeding period, We further hypothesise that P. australiensis has a could suffer higher mortality of its young under fecundity advantage and M. australiense a size and disturbed and unpredictable conditions (Winemiller movement advantage, which may allow persistence & Rose, 1992; Winemiller, 2005). There is evidence under altered flow conditions, but C. mccullochi has from the Campaspe River study that the production of neither. Further studies, to investigate the swimming M. australiense is reduced in the most regulated abilities of C. mccullochi at various life stages, intra- sections of that river, but this is possibly more a and inter-annual variation in recruitment and rela- function of the effect of reduced water temperature on tionships between recruitment and key environmental growth than of reproductive success (Richardson variables, especially flow, are needed. et al., 2004). However, species with equilibrium traits It is possible that the longer breeding period of may be able to persist in altered environments if they P. australiensis may also provide a recruitment advan- have the opportunity and ⁄or ability to avoid tempo- tage for this species. An earlier study indicated that rarily unfavourable conditions through movement. P. australiensis usually bred for at least 1 month longer Juvenile and adult M. australiense are known to be than C. mccullochi (Richardson et al., 2004). The pro- able to swim against considerable current velocities tracted spawning period of some small, short-lived (Fielder, 1970; Lee & Fielder, 1984) and to prefer main species of fish has been suggested as a reason for their channel habitats (Richardson & Cook, 2006); therefore, persistence in rivers in the Murray–Darling Basin with combined with their greater size and propensity for seasonally reversed flows (Humphries et al., 2002), a movement when very young (Price & Humphries, suggestions based largely on a hypothesis regarding 2010), it is possible the species can find more favour- recruitment success or failure of marine fish (Cushing, able conditions in rivers experiencing unpredictable 1990). If the peak production of young fish or shrimp conditions, such as aseasonal flow changes. Paratya coincides with peak production of their food, then australiensis can also swim against flow at adult and there is a good match and good recruitment should juvenile stages (Hancock & Bunn, 1999). result; but, if peaks in production of young and their The life history of the third species, C. mccullochi,is food do not match, then poor recruitment should intermediate between the other two and has neither result. A more protracted breeding period would the fitness advantage of high fecundity nor large size provide an advantage in a less predictable environ- or rapid larval development. The species is largely ment (one altered from long-term patterns) because it confined to slow-flowing and still habitats in lowland is more likely that at least some young will encounter rivers throughout its life (Richardson & Cook, 2006), favourable conditions for recruiting. which suggests poor swimming ability (although this Our study found similar fluctuations in fecundity, has not been studied), making it vulnerable to egg size and reproductive output throughout the unpredictable or aseasonal flow events (e.g. see respective breeding periods of three co-existing Humphries et al., 2006), especially during the breed- shrimp species in an Australian lowland river. ing period. There were, however, considerable differences in the Without regulation, discharge in lowland rivers in absolute values of these traits among the three species. the south-eastern region of the Murray–Darling Basin Moreover, interspecific differences can explain the

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 2011–2022 2020 A. Richardson and P. Humphries patterns in abundance and distribution of the species transition in phylogeographic diversification. Molecular in the heavily regulated Campaspe River and are Biology, 15, 1083–1093. consistent with the current tenets of life history theory Cushing D.H. (1990) Plankton production and year-class and how they relate to environmental disturbance. strength in fish populations: an update of the Based on our study in the Broken River and on the match ⁄mismatch hypothesis. Advances in Marine Biol- ogy, 26, 249–293. three species of shrimps, we have generated several Diaz A.M., Alonso M.L. & Gutie´rrez M.R. (2008) Biolog- hypotheses that warrant testing on other species and ical traits of stream macroinvertebrates from a semi- in other rivers. Furthermore, reproductive traits are arid catchment: patterns along complex environmental only a subset of the factors that may vary among the gradients. Freshwater Biology, 53, 1–21. species we studied; with feeding, behaviour and Fielder D.R. (1970) The larval development of Macrobrach- physiological tolerances all potentially differing. ium australiense Holthius, 1950 (, Palaemoni- However, reproductive traits are undoubtedly subject dae) reared in the laboratory. Crustaceana, 18, 60–74. to high selection pressure during evolution (Lytle, Fryer G. (1977) Studies of the functional morphology and 2001; Lytle & Poff, 2004) and, therefore, their inves- ecology of the atyid prawns of Dominica. Philosophical tigation in other riverine organisms under altered Transactions of the Royal Society of London B: Biological flow conditions is likely to yield considerable under- Sciences, 277, 57–129. standing and assist in their management. Gayraud S., Statzner B., Bady P., Haybach A., Scho¨ll F., Usseglio-Polatera P. & Bacchi M. (2003) Invertebrate traits for the biomonitoring of large European rivers: Acknowledgments an initial assessment of alternative metrics. Freshwater Biology, 48, 2045–2064. We thank Amina Price for reviewing early drafts and Gehrke P.C., Brown P., Schiller C.B., Moffat D.B. & Bruce providing advice on statistical analyses. This project A.M. (1995) River regulation and fish communities in was supported by a grant from Environment Austra- the Murray–Darling River System, Australia. Regulated lia and further assistance provided by the Murray– Rivers: Research & Management, 11, 363–375. Darling Freshwater Research Centre. Griswold M.W., Berzinis R.W., Crisman T.L. & Golladay S.W. (2008) Impacts of climatic stability on the struc- tural and functional aspects of macroinvertebrate References communities after severe drought. Freshwater Biology, Anger K. & Moreira G.S. (1998) Morphometric and 53, 2465–2483. reproductive traits of tropical caridean shrimps. Jour- Hancock M.A. & Bunn S.E. (1997) Population dynamics nal of Biology, 18, 823–838. and life history of Paratya australiensis Kemp, 1917 Bauer R.T. (2004) Remarkable Shrimps. University of (Decapoda: Atyidae) in upland rainforest streams, Oklahoma Press, Norman, U.S.A. south-eastern Queensland, Australia. Marine and Fresh- Benzie J.A.H. (1982) The complete larval development of water Research, 48, 361–369. Caridina mccullochi Roux, 1926 (Decapoda, Atyidae) Hancock M.A. & Bunn S.E. (1999) Swimming response to reared in the laboratory. Journal of Crustacean Biology, 2, water current in Paratya australiensis Kemp, 1917 493–513. (Decapoda, Atyidae) under laboratory conditions. Bongers T. (1990) The maturity index: an ecological Crustaceana, 72, 313–323. measure of environmental disturbance based on nem- Hancock M.A., Hughes J.M. & Bunn S.E. (1998) Influence atode species composition. Oecologia, 83, 14–19. of genetic and environmental factors on egg and clutch Bunn S.E. & Arthrington A.H. (2004) Basic principles and sizes among populations of Paratya australiensis Kemp ecological consequences of altered flow regimes for (Decapoda: Atyidae) in upland rainforest streams, aquatic biodiversity. Environmental Management, 30, south-east Queensland. Oecologia, 115, 483–491. 492–507. Humphries P., Serafini L.G. & King A.J. (2002) River Clarke A. (1993) Reproductive trade-offs in caridean regulation and fish larvae: variation through space and shrimps. Functional Ecology, 7, 411–419. time. Freshwater Biology, 47, 1307–1331. Cook B.D., Baker A.M., Page T.J., Grant S.C., Fawcett Humphries P., Cook R.A., Richardson A.M. & Serafini J.H., Hurwood D.A. & Hughes J.M. (2006) Biogeo- L.G. (2006) Creating a disturbance: manipulating graphic history of an Australian freshwater shrimp, slackwaters in a lowland river. River Research and Paratya australiensis (Atyidae): the role life history Applications, 22, 525–542.

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