Aquatic Sciences

, Volume 72, Issue 3, pp 335–346

Hyporheic annelid distribution along a flow permanence gradient in an alluvial river

Authors

    • MALY, Lyon, Cemagref
  • M. Lafont
    • MALY, Lyon, Cemagref
  • S. T. Larned
    • National Institute of Water and Atmospheric Research Ltd.
Research Article

DOI: 10.1007/s00027-010-0139-6

Cite this article as:
Datry, T., Lafont, M. & Larned, S.T. Aquat. Sci. (2010) 72: 335. doi:10.1007/s00027-010-0139-6

Abstract

In this study, we examined hyporheic annelid assemblages along a gradient of flow permanence (FP) and compared assemblages in gaining (groundwater-fed) and losing (runoff-fed) sections of the alluvial Selwyn River, New Zealand. To reduce the effects of poor taxonomic resolution, we used a dataset with most taxa identified to the genus or species level. We predicted that annelid assemblages would vary in structure and composition along FP gradients due to differences in desiccation resistance between taxa. We also predicted that groundwater-fed (gaining) and runoff-fed (losing) river sections would be inhabitated by dissimilar annelid assemblages due to differences in river-aquifer connections and recolonization sources. We found a negative relationship between taxon richness and FP, indicating that, on average, two annelid taxa are lost from hyporheic assemblages in the Selwyn River with every 10% decrease in FP. Low FP appears to favour annelid taxa that tolerate moist or dry conditions in sediments, as shown by a negative relationship between FP and the proportion of desiccation-tolerant taxa. A high proportion of hypogean taxa distinguished the groundwater-fed and perennial-gaining reach from the other reaches. In spite of the large differences in physical structure between the intermittent-gaining and the ephemeral-losing reach, we found few between-reach differences in annelid assemblages and, in particular, no differences in % hypogean taxa. These varied results illustrate the need to employ both categorical and continuous variables in ecological analyses: the combined categorical and gradient approach used in the present study is likely to explain more variability than either univariate approach alone.

Keywords

OligochaetesInterstitial sedimentsDryingSW–GW exchangesLongitudinal patternsTemporary river

Introduction

Intermittent and ephemeral (hereafter, “temporary”) rivers comprise a large proportion of the total number, length and discharge of the world’s rivers (Tooth 2000). Temporary rivers occur in all climatic regions and many geological terrains (Larned et al. 2009). Flow intermittence in these rivers controls or influences the composition and abundance of microbial, algal, invertebrate and fish assemblages (Stanley et al. 2004; Acuña et al. 2005; Davey and Kelly 2007; Larned et al. 2007). Benthic invertebrates have been the best-studied assemblages in temporary rivers. Results of studies across a wide range of climatic and geological settings indicate that benthic invertebrate abundance and diversity in temporary rivers are strongly influenced by flow permanence (FP; the proportion of time that water is present) (Burgherr et al. 2003; Wood et al. 2005; Stubbington et al. 2009; Arscott et al. 2010). Studies of hyporheic invertebrate assemblages in temporary rivers are far rarer than those for benthic invertebrates. Correlations between hyporheic invertebrate assemblages and FP and surface water–groundwater exchange have been reported for a single temporary river in New Zealand (Datry et al. 2007). Those correlations reflected differences between hyporheic taxa in desiccation tolerance, affinity with groundwater, and colonization sources (e.g., aquifers, runoff-fed tributaries). Conclusions from the New Zealand study were constrained by taxonomic resolution and the same issues hinder hyporheic and phreatic studies worldwide (Strayer 1994; Marmonier 1997; Malard et al. 2003a; Scarsbrook et al. 2003). Most studies of hyporheic invertebrate assemblages in both perennial and temporary rivers are based on datasets composed of mixed taxonomic levels (Malard et al. 2001; Olsen and Townsend 2005; Datry et al. 2007). This variation in taxonomic resolution can confound relationships between assemblage structure and environmental conditions (Alpert 2005; Watanabe 2006).

Annelids are common in virtually all aquatic systems, including temporary rivers (Stanley et al. 1994; Malard et al. 2001; Williams 2006; Datry et al. 2007; Stubbington et al. 2009). Annelids are particularly abundant in hyporheic zones, where they can account for >50% of the macrofauna in perennial rivers (Lafont and Malard 2001; Fowler and Scarsbrook 2002) and >20% of the macrofauna in temporary rivers (Datry et al. 2007; Stubbington et al. 2009). Since they lack aerial stages and have limited mobility in water, annelids have low dispersal capacities compared with other aquatic invertebrate groups in temporary rivers. The combination of high abundance and limited dispersal suggests that many annelid taxa in temporary rivers are physiologically adapted to desiccation. While experimental analyses of desiccation effects on annelids are rare, formation of thick-walled cysts and cocoons have been reported for many species, and these traits may confer desiccation resistance (Montalto and Marchese 2005; Williams 2006). Results from studies in which dry sediment from temporary rivers and floodplains was rewetted support the view that annelids can dominate invertebrate assemblages through desiccation resistance (Paltridge et al. 1997; Larned et al. 2008; Stubbington et al. 2009). In these studies, annelids were among the most numerous taxa following rewetting. However, no inferences could be drawn about variation among annelid taxa in desiccation resistance or colonization potential due to coarse taxonomic resolution.

Surface water–groundwater exchange is an important source of hydrological variation in alluvial rivers. High rates in gains from and losses to aquifers can create alternating perennial, ephemeral and intermittent reaches along river corridors (Lake 2003; Doering et al. 2007; Larned et al. 2008). The terms ephemeral and intermittent are used here to distinguish two types of temporary river reaches: ephemeral reaches only receive runoff because the channel is always above the groundwater table; intermittent reaches receive groundwater when the water table intersects the channel, and may also receive runoff. Perennial, ephemeral and intermittent reaches can have dissimilar flow regimes and physico-chemical conditions, and consequently, dissimilar invertebrate assemblages (Stanford and Ward 1993; Lafont and Malard 2001; Datry et al. 2007; Arscott et al. 2010).

Ephemeral and intermittent reaches can also differ in the quality and availability of wetted refugia for invertebrates with limited dispersal capabilities, such as annelids. During channel drying, hyporheic zones in ephemeral reaches contract rapidly, while those in intermittent reaches contract slowly or not at all while a saturated connection to the water table exists (Wroblicky et al. 1998; Boulton 2003; Datry and Larned 2008). Upward migration of groundwater taxa from underlying aquifers can be an important colonization pathway in intermittent reaches, whereas colonization of the hyporheic interstices after rewetting in ephemeral reaches is largely restricted to surface taxa. Annelids are known to undergo vertical migrations between hyporheic zones and deeper aquifers, and it is likely that aquifers are colonization sources for hyporheic zones in gaining (upwelling) river reaches, but not in losing (downwelling) reaches (Malard et al. 2001, 2003b). As with most studies of invertebrate responses to flow intermittence, studies of hyporheic invertebrate responses to surface water–groundwater exchange are generally based on datasets composed of mixed taxonomic levels (e.g., Brunke and Gonser 1999; Fowler and Scarsbrook 2002; Datry et al. 2007).

In the present study, we examined hyporheic annelid assemblages along a gradient of FP and compared assemblages in groundwater-fed and runoff-fed river sections. To reduce the effect of poor taxonomic resolution, we used a dataset with most taxa identified to the level of genus or species. We tested two predictions, which were based on results of previous comparisons of lotic invertebrates in perennial and temporary reaches, and in groundwater-fed and runoff-fed reaches. The first prediction was that annelid assemblages vary in structure and composition along FP gradients due to differences in desiccation resistance between taxa. The second prediction was that groundwater-fed (gaining) and runoff-fed (losing) river sections would be inhabitated by dissimilar annelid assemblages due to differences in river-aquifer connections and recolonization sources.

Methods

Study location

The study was conducted in the alluvial Selwyn River, South Island, New Zealand. The Selwyn River flows through the foothills of the Southern Alps, then east for 58 km across and under the Canterbury Central Plains to coastal Lake Ellesmere (Fig. 1). The 2,800 km2 Central Plains extend from the foothills east to the Pacific Ocean, and are bounded on the north by the Waimakariri River and on the south by the Rakaia River (Fig. 1a). The plains are composed of glacial and fluvial greywacke gravels and, near the coast, additional layers of marine sediments deposited during high sea stands (Larned et al. 2008). The Selwyn River flows down a depression between the alluvial fans of the Waimakariri and Rakaia Rivers.
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Fig. 1

Location of the Selwyn River on the South Island of New Zealand (a), and the Selwyn River mainstem showing location of 16 cross-sections used in the study (b). Dotted lines indicate borders between river reaches and geomorphic regions described in the text

In the western (inland) region of the Central Plains, alluvial aquifers are poorly unconfined and the regional water table is 15–50 m below ground surface. The Selwyn River is perched in this region, and transmission losses to the underlying aquifers are high (Rupp et al. 2008). Due to progressive losses, the flow regime shifts from perennial to ephemeral within 3 km of the foothills. In the eastern (coastal) region of the plains, alluvial aquifers are confined and the shallowest aquifers are at or near ground surface. In this region, the Selwyn River is gaining, and groundwater inflow causes the flow regime to shift from intermittent to perennial ~5 km from Lake Ellesmere (Fig. 1). The arrangement of poorly-confined and highly-confined aquifers, and longitudinal flow losses and gains create four abutting reaches across the Canterbury Plains: a perennial-losing reach, an ephemeral-losing reach, an intermittent-gaining reach and a perennial-gaining reach (Fig. 1). In most years, the river first dries in late spring/early summer near the boundary between the ephemeral and intermittent reaches, and the dry segment expands upstream and downstream towards the perennial reaches. Progressive drying creates a longitudinal FP gradient, weakly affected by tributary inflows that create longitudinal discontinuities. A detailed description of the Selwyn River environment is given in Larned et al. (2008).

Sixteen sampling sites (3 perennial, 13 ephemeral and intermittent) were established at 1.4–7.1 km intervals along the 56-km long river mainstem, from the foothills–plains boundary to a point 8 km upstream of Lake Ellesmere (Fig. 1). The presence or absence of flow at each sampling site was recorded at 2-week intervals from October 2003 to July 2005, and FP was estimated as the ratio of observed days of flow to total observation days. FP at the sampling sites ranged from 7 to 100% (Larned et al., 2008).

Sample collection and processing

Hyporheic samples were collected on 16 dates between January 2003 and July 2005. The sampling procedure is described in detail in Datry et al. (2007). Briefly, samples were collected >1 m from the channel edge at each flowing cross-section, and replicate samples were spaced ca. 2-m apart; 1–5 samples were collected at each site and date, depending on cross-section width. All samples were taken from riffle tails to reduce effects of small-scale habitat variability. Samples were only collected when water depth over the riffle tails was >30 cm. The number of cross-sections sampled on each date ranged from 3 to 16, depending on the presence and length of the dry central segment. Samples were collected at 3-month intervals, on average (minimum interval 1 month), to minimize disturbance effects on subsequent sampling dates. Hyporheic samples were collected using temporary PVC piezometers, which were removed after each sample collection. The piezometers (2 cm inside diameter) were driven 30 cm below the sediment surface with a hardened steel driving rod, and then 4 L of hyporheic water were withdrawn from the pipes at a constant rate with a bilge pump, then filtered through a 63-μm mesh sieve. Annelids retained on the sieve were preserved in 70% isopropyl alcohol, and identified to the lowest possible taxonomic level (class for Aphanoneura, and family, genus or species for Oligochaeta) using keys in Nielsen and Christensen (1959) and Brinkhurst and Jamieson (1971). Most of the annelid taxa were then classified as epigean or hypogean. Epigean taxa included stygoxen and occasional hyporheos, and hypogean taxa included permanent hyporheos and stygobites, as defined in Gibert et al. (1994) and Scarsbrook et al. (2003). Some taxa could not be reliably classified due to gaps in natural history information; 79% of the taxa could be classified reliably. Taxa were also classified as tolerant or sensitive to desiccation, based on information in Nielsen and Christensen (1959), Brinkhurst and Jamieson (1971), Brinkhurst and Gelder (2001), and unpublished information; 49% of the taxa could be classified reliably.

Data analysis

Annelid assemblages were characterized using the following variables: density (number of individuals per 4-L sample), taxon richness (number of taxa per 4-L sample), frequency of occurrence (number of samples containing a given taxon divided by the total number of samples (95 in total)), relative abundance (total number of individuals of a taxon divided by the total number of annelids), percent hypogean, percent desiccation-tolerant, and Simpson’s diversity index (1−D), where \( D = {\frac{1}{{\sum\nolimits_{i = 1}^{S} {p_{i}^{2} } }}}, \)S is the total number of annelid taxa in the assemblage (taxon richness), and pi is the proportion of S made up of the ith taxon. Relationships between FP and annelid assemblage variables were analyzed by linear regression. Comparisons of assemblage variables among reach types (perennial-losing, ephemeral-losing, intermittent-gaining, perennial-gaining) were made by 1-way ANOVA and post-hoc Scheffé comparisons, using sampling dates as replicates. Data normality was checked with Smirnov–Kolmogorov tests. Relative abundances were arcsine-transformed prior to analysis. The significance level for all statistical analyses was 0.05.

Differences in annelid assemblage structure among reaches were assessed with a between-groups principal component analysis (PCA), using log-transformed annelid densities. Between-groups PCAs generate axes that correspond to the center of gravity among all groups, which provides a representation of the spatial discrimination of sites. The significance of the proportion of the variability explained by site differences was tested by Monte-Carlo permutation (Dolédec and Chessel 1989). The PCA was calculated and ordinations prepared using the ADE-4 software package for R (Thioulouse et al. 1997).

Results

Annelid assemblages

Annelids were present in 93% of the hyporheic samples, and were dominated numerically by individuals in the Subclass Oligochaeta and Class Aphanoneura. In total, 1,458 oligochaetes (75% relative abundance) and Aphanoneura (15% relative abundance) comprising 44 taxa were collected from the 16 sampling sites (Table 1). Pristina osborni, Aphanoneura and Cernosvitoviella spp. were the most frequent taxa with 53.7, 46.3 and 45.3% occurrence, respectively (Table 1). The average density was 14 annelids per 4-L sample (range: 1–65, n = 95), and the three most frequently encountered taxa represented 48% of all individuals collected. The 12 least abundant taxa each occurred in a single sample.
Table 1

List of hyporheic Oligochaete and Aphanoneura taxa in the Selwyn River, with taxa code used in the PCA

Species

PCA code

Habitat

DR

TI

RA (%)

FO (%)

NAIDIDAE (Tubificinae)

 Aulodrilus pluriseta (Piguet 1906)

AUPL

EPI (1)

NR

3

0.2

3.2

NAIDIDAE (Rhyacodrilinae)

 Rhyacodrilus lindbergi Hrabem, 1963

RHLI

HYPO (2)

NR

5

0.3

3.2

 Rhyacodilus sp.

RHSC

HYPO (3)

NR

1

0.0

1.1

NAIDIDAE (Phallodrilinae)

 Phallodrilus sp. (immature worms)

PHOO

HYPO (3)

NR

3

0.2

3.2

NAIDIDAE (Pristininae)

 Pristina amphibiotica Lastockin, 1927

PRAM

HYPO (3)

NR

88

6.1

7.4

 Pristina osborni (Walton 1906)

PROS

HYPO (3)

NR

305

21.0

53.7

 Pristina breviseta Bourne, 1891

PRBR

HYPO (3)

NR

143

9.8

28.4

 Pristina aequiseta Bourne, 1891 form foreli

PRFO

HYPO (3)

NR

34

2.3

14.7

 Pristina aequiseta Bourne, 1891 form aequiseta

PRAQ

HYPO (3)

NR

19

1.3

13.7

 Pristina jenkinae Stephenson, 1931

PRJE

HYPO (3)

T

68

4.7

23.2

 Stephensoniana trivandrana (Aiyer 1926)

STTR

HYPO (3)

NR

2

0.1

1.1

NAIDIDAE (Naidinae)

 Chaetogaster diaphanus (Gruithuisen, 1828)

CHDI

EPI (1)

I

12

0.9

9.5

 Chaetogaster diastrophus (Gruithuisen, 1828)

CHDS

EPI (1)

I

16

1.1

11.6

 Specaria josinae (Vejdovsky, 1883)

SCJO

EPI (1)

I

1

0.0

1.1

 Nais communis Piguet, 1906 (with eyes)

NAC1

EPI (1)

I

6

0.4

5.3

 Nais communis Piguet, 1906 (eyeless)

NAC2

HYPO (4)

NR

90

6.2

32.6

 Nais christinae Kasprzak, 1973

NACH

EPI (5)

I

13

0.9

6.3

 Nais elinguis Muller, 1773

NAEL

EPI (1)

I

42

2.9

15.8

 Nais simplex Piguet, 1906

NASI

EPI (1)

I

1

0.1

1.1

 Nais variabilis Piguet, 1906

NAVA

EPI (1)

I

18

1.2

7.4

 Slavina appendiculata d’Udekem, 1855

SLAP

EPI (1)

I

1

0.1

1.1

ENCHYTRAEIDAE

 Cernosvitoviella spp. (immature worms)

CEOO

HYPO (3)

NR

126

8.6

45.3

 Cernosvitoviella atrata (Brestscher, 1903)

CEAT

HYPO (3)

NR

2

0.1

3.2

 Marionina argentea (Michaelsen, 1889)

MAAR

HYPO (3,6)

NR

88

6.1

23.2

 Marionina subterranea (Knöllner, 1935)

MASU

HYPO (7)

NR

16

1.1

6.3

 Fridericia sp. 1

FRO1

NR

NR

1

0.1

1.1

 Fridericia sp. 2

FRO2

NR

NR

2

0.1

2.1

 Cognettia sp.

COOO

NR

NR

5

0.3

4.2

 Enchytraeidae gr.1

ENC1

NR

T

17

1.2

7.4

 Enchytraeidae gr.4

ENC4

NR

T

48

3.3

13.7

 Enchytraeidae gr.5

ENC5

NR

T

2

0.1

1.1

 Enchytraeidae gr.6

ENC6

NR

T

1

0.1

1.1

LUMBRICULIDAE

 Lumbriculidae, g. sp. (immature worms)

STOO

HYPO (3)

NR

7

0.5

8.4

 Lumbriculus variegatus (Muller, 1773)

LUVA

EPI (1)

NR

1

0.0

1.1

LUMBRICIDAE

 Lumbricidae g. sp.

LUBC

EPI (1)

T

1

0.1

2.1

PHREODRILIDAE

 Phreodrilidae immature worms BM

PRbm

HYPO-EPI (8)

I

28

1.9

21.1

 Phreodrilidae g. sp.1 BM, presence of a proboscis

ANPR

HYPO-EPI (8)

I

2

0.1

1.1

 Phreodrilidae immature worms 2 M

PS2m

HYPO-EPI (8)

I

2

0.1

2.1

 Phreodrilidae g. sp.2 2 M, mature worms

PSSU

HYPO (8)

I

3

0.2

3.2

 Phreodrilidae g. sp.3 mature worms 2 M, penial sheath

PSGS

HYPO-EPI (8)

I

2

0.1

2.1

 Phreodrilidae g. sp.4 2 M, mature worms

PSCR

HYPO-EPI (8)

I

1

0.1

1.1

 Phreodrilidae immature worms 2B

PS2b

HYPO-EPI (8)

I

9

0.6

10.5

 Phreodrilidae g. sp.5 2B, mature worms

INLA

HYPO-EPI (8)

I

4

0.3

4.2

APHANONEURA

 Aphanoneura g. spp.

APHN

HYPO-EPI (6)

I

217

14.9

46.3

Unidentified Annelida

INCE

NR

NR

1

0.1

1.1

Types of Phreodrilidae; BM ventral bundles with one simple-pointed and one bifid crotchets; 2M ventral bundles with two simple-pointed crotchets; 2B ventral bundles with two bifid crotchets; the used nomenclature conformed to the last ICZN rules (Erséus et al. 2008); (1) Brinkhurst and Jamieson (1971); (2) Creuze-des-Châteliers et al. (2009); (3): Lafont and Vivier (2006); (4): Lafont and Malard (2001); (5) Kasprzak (1973); (6) Juget and Dumnicka (1986); (7) Nielsen and Christensen (1959); (8) Brinkhurst (1990); Pinder (2008); Pinder and Brinkhurst (1997); Pinder and Erséus (2000)

EPI epigean, HYPO hypogean, DR desiccation resistance, U undetermined, NR non resistant, R resistant, TI total individuals, RA: relative abundance, FO frequency of occurrence

Pristina spp. was the most abundant taxon (657 specimens), followed by species in the Enchytreaidae (308 specimens) and Naidinae families (200 specimens). The presence of Stephensonianatrivandrana (Family Pristininae) was noteworthy because this species has not been previously reported from Australia or New Zealand. Another noteworthy result was the collection of 90 specimens of the eyeless form of Nais communis (see “Discussion”).

Effects of flow permanence

Annelid taxon richness and Simpson diversity increased with increasing FP, and reached maximum values at near-perennial and perennial sites in both the losing (inland) and gaining (coastal) river sections (Fig. 2a, c). The proportion of desiccation-tolerant taxa decreased with increasing FP, with an average of 4% at perennial sites and 38% at the most ephemeral site (Fig. 2d). The proportion of epigean taxa increased logarithmically with FP, from 20% at perennial sites to 100% at the most ephemeral site (Fig. 2e). The proportion of hypogean taxa increased linearly with increasing FP, from 0% at the most ephemeral site to 80% at perennial sites (Fig. 2f). Note that 21% of the species could not be assigned to either one of the habitat categories. There was no detectable statistical relationship between annelid density and FP (Fig. 2b).
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Fig. 2

Relationships between hyporheic oligochaete assemblages and flow permanence in the Selwyn River. Lines and equations correspond to significant regressions

Differences among river reaches

There were no statistically significant differences in total density among river reaches (Fig. 3a). There was no significant difference in taxon richness between the perennial-losing and perennial-gaining reaches, but taxon richness was higher in the ephemeral reach (mean 4.3 taxa per sample) than in other reaches (Fig. 3b, Scheffé test, p < 0.05). The proportion of hypogean taxa was higher in the perennial-gaining reach (84%) compared to the perennial-losing reach (58%, Scheffé test, p = 0.014) and the temporary reaches (60%, Scheffé test, p = 0.019) (Fig. 3c). The proportion of epigean taxa was higher in the perennial-losing reach (32%) compared to the perennial-gaining reach (15%, Scheffé test, p = 0.001) and the temporary reaches (21%, Scheffé test, p = 0.001) (Fig. 3d). No significant differences between the ephemeral and intermittent reaches in proportions of hypogean or epigean taxa were detected (Fig. 3c, d), and no between-reach differences in proportions of desiccation-tolerant species were detected (Fig. 3e). Simpson diversity was higher in the perennial-losing reach than in the intermittent reach (Scheffé test, p = 0.001), but no other differences among reaches were detected (Fig. 3f).
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Fig. 3

Boxplots (median ± 25–75% quartiles) showing the distribution of hyporheic oligochaete assemblage characteristics among the four reach types. PL permanent losing, PG permanent gaining, EphL ephemeral losing, and IntG intermittent gaining. On each panel, different letters added to the different boxes indicate significant statistical differences

Oligochaete assemblage composition

The between-groups PCA indicated that annelid assemblage structure varied among the four Selwyn River reaches (Monte Carlo permutation, p < 0.001), although a small proportion of the total variance was explained by reach types (14%). Axis 1 accounted for 50.6% of the between-group variance and axis 2 for 29.6%. Annelid taxa formed three distinct groups on the ordination (Fig. 4a). Group 1, on the positive sides of axes 1 and 2, was dominated by Phallodrilus sp., Aulodrilus pluriseta, Rhyacodrilus lindbergi, Rhyacodilus sp., Specaria josinae, and Pristina aequiseta (form aequiseta). Group 2, on the positive side of axis 1 and the negative side of axis 2, was dominated by Cernosvitoviella spp., Phreodrilidae, Lumbriculidae g. sp., unidentified annelid, Lumbriculus variegatus, Nais communis (eyed) and Insulodrilus lacustris. Group 3, on the negative side of axis 1 and the positive side of axis 2, was dominated by unidentified aphanoneurans, Enchytraeidae gr.4, Pristina breviseta, Marionina argentea, Pristina aequiseta (form foreli), Nais elinguis, Marioninasubterranea, Chaetogaster diaphanus and Chaetogaster diastrophus. A single taxon (Nais communis (eyeless form) was located outside of the 3 taxa groups, on the negative sides of both axes (Fig. 4a). The sampling sites were distributed in the ordination along an intermittence gradient, with perennial sites on the positive side of Axis 1 and the most ephemeral and intermittent sites on the negative side (Fig. 4b). Axis 2 separated perennial sites, with perennial-losing sites on the positive side of the axis, and perennial-gaining sites on the negative side (Fig. 4b).
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Fig. 4

Between-groups PCA of hyporheic oligochaete data using log(x + 1)-transformed densities. a Ordination diagram of taxa (Factor 1 × Factor 2). b Mean factorial scores of sites. PL permanent losing, PG permanent gaining, EphL ephemeral losing, and IntG intermittent gaining. See Table 1 for taxa codes

Relative abundances of taxa from PCA Group 1 were significantly higher in the perennial-losing reach than in the other reaches (p < 0.05, Scheffé tests, Fig. 5). These taxa represented ~40% of the total abundance in the perennial-losing reach, and <10% in the other reaches. In contrast, relative abundances of taxa from PCA Group 2 were significantly higher in the perennial-gaining reach (p < 0.05, Scheffé tests, Fig. 5). These taxa represented ~25% of total abundances in the perennial-losing reach, and <3% in the other reaches. Relative abundances of taxa from PCA Group 3 were significantly higher in ephemeral and intermittent reaches than in perennial reaches (p < 0.05, Scheffé tests, Fig. 5). There were no detectable differences between the ephemeral and intermittent reaches in relative abundances of Group 3 taxa. The relative abundance of eyeless Nais communis was higher in the perennial-gaining reach than in the other reaches (p < 0.05, Scheffé tests).
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Fig. 5

Boxplots (median ± 25–75% quartiles) showing the distribution of % species belonging to the three groups identified previously from the PCA among the four section types. PL permanent losing, PG permanent gaining, EphL ephemeral losing, and IntG intermittent gaining. On each panel, different letters added to the different boxes indicate significant statistical differences

Discussion

Annelid assemblages and flow permanence

We predicted that annelid assemblages vary in response to FP along the Selwyn River and our results supported this prediction. The negative relationship between taxon richness and FP indicated that, on average, two annelid taxa were lost from hyporheic assemblages in the Selwyn River with every 10% decrease in FP. Low FP appears to favour annelid taxa that tolerate moist or dry conditions in sediments, as indicated by the negative relationship between FP and the proportion of desiccation-tolerant taxa. However, <50% of the Oligochaete taxa sampled could be assigned to a desiccation-resistance class with certainty, so the relationship between FP and the prevalence of desiccation-tolerant taxa is tentative. Effects of FP on life-history traits that confer resistance to drying and/or resilience following dry periods in the Selwyn River are more apparent in benthic invertebrate assemblages than in hyporheic oligochaetes. An analysis of benthic invertebrates from the Selwyn indicated that proportions of taxa corresponding to nine life-history traits associated with desiccation resistance or resilience varied directly with FP (Arscott et al. 2010). Benthic invertebrates on exposed channel surfaces may be more sensitive to changes in FP than hyporheic invertebrates in sediment interstices, but more information about taxon-specific traits in hyporheic invertebrates, particularly annelids, is needed to test that proposition. While information about life-history traits in freshwater annelids is scarce, observations of encystment, pupation, and inducible osmolyte production in annelids from drying soils, wetlands, floodplains and streams suggest that flow intermittence can favour taxa with appropriate traits (Cook 1969; Kaster and Bushnell 1981; Marchese 1987; Anlauf 1990; Montalto and Marchese 2005).

In laboratory inundation experiments using sediments from a wide range of temporary rivers, annelids were among the most abundant surviving hyporheic taxa (Boulton and Lloyd 1992; Tronstad et al. 2005; Larned et al. 2008; Stubbington et al. 2009). In field studies of recolonization following resumption of flow in temporary streams, annelids were among the first colonists to emerge from sediments (Williams and Hynes 1976; Williams 1977). These observations confirm that annelids from some taxa are capable of persisting in hyporheic zones during prolonged dry periods. However, the marked effects of intermittence on annelid taxonomic composition in the Selwyn River also indicate that river drying acts as an environmental filter by progressively eliminating desiccation-sensitive taxa. While the mechanism by which this filter acts is not known, we can presume that it involves physiological and reproductive stress that in turn affects survivorship of sensitive taxa.

Physiological and reproductive responses to desiccation have recently been characterized in oligochaetes from the family Enchytraedae (Maraldo et al. 2009). Species from this family are among the most widespread annelids in the Selwyn River hyporheic zone (Table 1). Maraldo et al. (2009) reported that several enchytraeid species resist dehydration during short dry periods (≤1 day) by maintaining high internal osmotic pressure. Prolonged (24–54 days) dry periods led to gradual dehydration and loss of osmotic pressure, and reduced survival and reproduction rates. Since enchytraeids were abundant at sites in the Selwyn River with dry periods >100 days, it is unlikely that these worms survived dry periods as adults. Instead, the hyporheic zone was probably recolonized by immigrants hatching from cocoons following each re-wetting. Aphanoneurans were also widespread and abundant in the Selwyn River hyporheic zone. Desiccation-resistance in these small (<1 mm length) annelids has been attributed to their ability to inhabit capillary films on sediment particles (Juget and Dumnicka 1986). However, sediment water content in dry portions of the Selwyn is generally <5% (Larned et al. 2007), and capillary water is not be present under these conditions. As with the enchytraeids, we predict that aphanoneurans persist in dry sediments by encystment, and become active upon rewetting.

We could reliably classify 80% of the annelid taxa sampled in the Selwyn River as hypogean or epigean, and we detected a negative relationship between the proportion of epigean taxa and FP. Sites with the lowest FP were in the ephemeral reach, and these sites were dominated by epigean taxa. Due to high rates of surface water loss in the ephemeral reach (up to 0.6 m3 s−1 km−1; Larned et al. 2008) and the deep unsaturated zone beneath the river channel, a permanent hyporheic zone does not occur in this reach. Recolonisation of hyporheic zones in ephemeral river reaches following rewetting appears to be dominated by epigean taxa that drift or crawl from upstream perennial reaches (Dieterich and Anderson 2000; Storey and Quinn 2008; Arscott et al. 2010).

Annelid assemblages and surface–subsurface exchange

Our second prediction was that annelid assemblage structure would differ among the four reach types (perennial-losing, ephemeral-losing, intermittent-gaining, perennial-gaining), and our results partly supported this prediction. For example, a high proportion of hypogean taxa distinguished the groundwater-fed, perennial-gaining reach from the other reaches. Characteristic obligate hypogean taxa in the perennial-gaining reach included the eyeless ecotype of Nais communis. The eyeless condition is considered one of a suite of adaptations in hypogean invertebrates, and eyeless N. communis have been reported from groundwater upwelling zones in other rivers (Lafont and Malard 2001; Lafont and Vivier 2006; Creuzé des Châtelliers et al. 2009). However, gaining and losing reaches did not differ statistically in annelid assemblage density or taxonomic richness. This was unexpected, given that Malard et al. (2001) and Lafont and Malard (2001) found higher hyporheic oligochaete taxonomic richness and density in gaining reaches compared to losing reaches of a glacial river (Val Roseg, Switzerland). In the Selwyn River, we may have lacked statistical power to detect comparable between-reach differences, due to within-reach variability and limited sample sizes.

Differences in colonization sources and in the availability of aquatic refugia during dry periods led us to expect corresponding differences in annelid assemblages in the ephemeral and intermittent reaches. Unsaturated zones always separate the hyporheic zone from the regional water table in ephemeral reaches. In contrast, a saturated connection periodically connects the hyporheic zone and water table in intermittent reaches. This connection is expected to provide a pathway for invertebrates moving between the channel and the aquifer in response to flow variation (Ward et al. 1998; Datry et al. 2008). During dry periods, hyporheic organisms, and particularly those lacking aerial stages (such as annelids), seek refuge in aquifers below intermittent river reaches (Brunke and Gonser 1997). In some ephemeral river reaches with fine-grained channel substrata, pools with low seepage rates can function as short-term refugia (Labbe and Fausch 2000). However, in rivers with coarse-grained substrata such as the Selwyn, high seepage rates preclude the formation of persistent pools in ephemeral reaches (Arscott et al. 2010).

Despite large differences in physical structure in the ephemeral and intermittent reaches of the Selwyn River, we found few between-reach differences in annelid assemblages. The most notable difference was higher average taxon richness at ephemeral sites compared with intermittent sites. The ephemeral reach (35-km long) is much longer than the intermittent reach (8-km), and included more sampling sites. Higher taxon richness may be due to the larger taxon pool that was sampled over the length of the ephemeral reach. The fact that we found no differences between the ephemeral and intermittent reach in % hypogean taxa was unexpected. We predicted that the proportion of hypogean taxa would be higher in the intermittent reach than in the ephemeral reach due to the saturated channel-aquifer connection in the intermittent reach. The lack of substantial differences between the intermittent and ephemeral reach with regards to the proportions of hypogean annelids in this study is consistent with the results of the previous study of Selwyn River hyporheos in which no between-reach difference in % hypogean invertebrates (all taxa combined) was detected (Datry et al. 2007). These results indicate that migration of hypogean invertebrates from aquifers to hyporheic zones does not always have a dominant effect on hyporheic assemblage structure, as previous observed in a glacial river study (Malard et al. 2001, 2003b). Taken together, the strong effects of FP on annelid assemblages, and the relatively minor differences between temporary reaches, suggest that temporal variation in surface water has an overriding effect on hyporheic annelids, whether the source of surface water is runoff (in ephemeral reaches) or aquifers (in intermittent reaches). The large-scale effects of FP may mask the effects of other environmental factors (e.g., grain size, organic matter content), which have been shown previously to influence small-scale hyporheic invertebrate distribution (Brunke and Gonser 1997; Weigelhofer and Waringer 2003).

As a broad generalization, the continuous variable FP explained a relatively large proportion of the variation in annelid assemblage structure, and categorical variables (i.e., river reaches) explained relatively little variation. This pattern was also observed in studies of fish and benthic invertebrates in the Selwyn River (Davey and Kelly 2007; Arscott et al. 2010), but contrasts with the previous studies of hyporheic and groundwater invertebrates and ecosystem processes (Datry and Larned 2008; Datry et al. 2008). In the latter studies, reach categories (perennial, intermittent, ephemeral) explained more variation in assemblage structure than continuous variables (flow, flow permanence, and distance downstream). Results of the current study suggest that annelid assemblages are sensitive to environmental changes that occur along longitudinal gradients (e.g., durations and frequencies of floods and intermittence), and less sensitive to qualitative changes such as river-aquifer exchange direction (gaining or losing) or groundwater connectivity (intervening unsaturated zone present or absent). The varied results of studies of different biotic components of a single river ecosystem illustrate the need to employ both categorical and continuous variables in ecological analyses. In most river ecology studies, the explanatory variables are exclusively categorical (e.g., habitat type) or continuous (e.g., flood frequency or magnitude). These univariate approaches limit the scope of inference and the amount of variation explained. The combined categorical and gradient approach used in the present study is likely to explain more variability than either univariate approach alone (Datry et al. 2007; Arscott et al. 2010).

Acknowledgments

We thank G. Cooper, M. Dale, G. Fenwick and M. Scarsbrook for assistance with fieldwork, P. Lambert for invertebrate identification, and G. Le Goff, R. Bonnard and C. Jézéquel for preparing annelid specimens. The authors thank Adrian M. Pinder (Department of Invertebrate Survey, Museum of Victoria, Abbotsford, Australia) for kind and stimulating discussions about the quickly evolving taxonomy of the Phreodrilidae Family. We also thank C. Robinson and two anonymous reviewers for comments and meticulous editing, which improved the final version of this paper. This project was funded by CEMAGREF and the New Zealand Foundation for Research, Science and Technology through the Water Allocation Programme (Contract C01X0308), the Groundwater Ecosystems Programme (Contract CO1X0503), and the Groundwater Allocation Programme (Contract LVLX0303).

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