Hydrobiologia

, Volume 801, Issue 1, pp 129–140 | Cite as

California vernal pool endemic responses to hydroperiod, plant thatch, and nutrients

  • Jamie M. Kneitel
  • Nestor Samiylenko
  • Luis Rosas-Saenz
  • Alyssa Nerida
CHALLENGES IN ANOSTRACAN RESEARCH

Abstract

Many endemic large branchiopods inhabit ephemeral freshwater ecosystems, including California vernal pools. Hydroperiod, inundation length, has been well studied in these systems that cycle between aquatic and terrestrial phases, but species’ responses to other ecological processes are still poorly known. For example, temporal (plant thatch from the previous terrestrial phase) and spatial (nutrient runoff) factors may have strong effects on emergence and population densities during the aquatic phase. We examined the effects of hydroperiod stability, thatch, and nutrients on the emergence and density of 4 vernal pool endemic species: Branchinecta lynchi (Anostraca), Linderiella occidentalis (Anostraca), Lepidurus packardi (Notostraca), and Cyzicus californicus (Spinicaudata). A full factorial mesocosm experiment was conducted which measured species densities, along with water quality variables. Hydroperiod and thatch differentially affected 3 of the 4 species based on emergence timing and life cycle. Treatments had effects on many water quality variables, and these variables were correlated with densities. These results highlight how hydroperiod stability along with other processes can affect large branchiopod species in temporary freshwater ecosystems. California vernal pools are a greatly reduced habitat rich in endemic and endangered species (including Branchinecta lynchi and Lepidurus packardi), and therefore, these results have implications for conservation and management.

Keywords

Anostraca Endangered species Notostraca Seasonal wetlands Spinicaudata 

Introduction

Temporary ponds and wetlands, freshwater ecosystems which experience an inundation–desiccation cycle, provide critical habitat for many species of large branchiopods, including Anostraca, Notostraca, and Spinicaudata (Hildrew, 1985; Eng et al., 1990; Williams, 2006; Brendonck et al., 2008; Waterkeyn et al., 2008; Van den Broeck et al., 2015; Boix et al., 2016). Distributed among the continents, these taxonomic groups survive harsh and variable conditions by producing resting egg stages that persist the dry phases of temporary aquatic environments (Hairston & Cáceres, 1996; Brendonck & DeMeester, 2003; Vanschoenwinkel et al., 2010a; Huang et al., 2010). Many large branchiopods exhibit high endemism levels and many are threatened or endangered (USFWS, 1996; Eng et al., 1990; Belk, 1998; Brendonck et al., 2008). Therefore, an ecological understanding of these species relies on identifying what conditions affect their emergence from the resting egg stage, as well as their population sizes (Jeffries, 2003).

Abiotic factors are well known for regulating populations and communities (Dunson & Travis, 1991), including large branchiopods (Waterkeyn et al., 2008; Olmo et al., 2015; Boix et al., 2016). Abiotic factors include pool depth (Hathaway & Simovich, 1996), pool size (Spencer et al., 1999), water chemistry (Waterkeyn et al., 2008), and water temperature (Waterkeyn et al., 2009). Hydroperiod, the length of inundation, is the predominant factor in structuring temporary pond communities (Hathaway & Simovich, 1996; Schneider & Frost, 1996, Tavernini et al., 2005; Brendonck et al., 2008; Waterkeyn et al., 2008; Vanschoenwinkel et al., 2010b, 2013; Kneitel, 2014; Brendonck et al., 2015; Zokan & Drake, 2015; O’Neill, 2016). Moreover, temporal factors such as the number of inundations (habitat stability), timing of inundation, and succession play an important role in the community structure of the ponds (e.g., Boix et al., 2004; Kneitel, 2014). In some cases, pool characteristics that change with inundation, like water chemistry, can be important in determining population densities and species composition (e.g., Nhiwatiwa et al., 2011).

Chemical composition of the aquatic environment has been shown to influence crustacean ecology upon emergence (Gannon & Stemberger, 1978; Williams, 2006; Waterkeyn et al., 2008; Florencio et al., 2014; Olmo et al., 2015; Van den Broeck et al., 2015). Anostracans, particularly, can be responsive to nutrient levels in the water, as with feeding changes in response to heightened nitrogen levels (Brendonck, 1993). Phosphate has also been implicated in species richness of temporary ponds (Waterkeyn et al., 2009). Other important variables affecting emergence and population sizes include conductivity and dissolved oxygen (Brendonck, 1996; Waterkeyn et al., 2009; Florencio et al., 2014; Van den Broeck et al., 2015). As temporary ponds in California are mainly located in highly agricultural areas (Holland, 1978), changes to water chemistry associated with runoff can also greatly affect California vernal pools (Smith et al., 1999; Kneitel & Lessin, 2010; Smolders et al., 2010).

The emergence of invertebrates from soil upon inundation can also be affected by physical structures in the habitat. Physical structure can decrease light, which can reduce species emergence from the soil egg bank (e.g., Pinceel et al., 2013). In natural wetland communities, plant thatch can increase light attenuation, increase structure, and change water chemistry, which have been well documented in plant communities (e.g., Facelli & Pickett, 1991; Weltzin et al., 2005). Since temporary freshwater ecosystems transition between aquatic and terrestrial habitats, plant thatch from the terrestrial phase can accumulate on the soil surface and affect the organisms of the aquatic community following inundation. These thatch effects on the aquatic invertebrate community have not been examined, and may occur directly through its physical presence or indirectly through chemistry changes with decomposition.

Mediterranean temporary ponds are ecosystems found in the Mediterranean climates of the world (Keeley & Zedler, 1998; Blaustein & Schwartz, 2001; Zacharias & Zamparas, 2010; Boix et al., 2016). They can be found in California in flat areas where a hardpan or other soil substrate prevents water percolation (Hobson & Dahlgren, 1998). The perched water table resulting from winter precipitation provides the hydrology of such ponds (Hanes & Stromberg, 1998; Rains et al., 2006). In spring, precipitation decreases and temperature increases, resulting in the evaporation of the ponds. Annual plants mostly dominate the terrestrial habitat through the spring (Collinge et al., 2011). Much of the summer and fall is the dry phase with little aboveground life occurring in these locations (Holland & Jain, 1981). California vernal pools support high levels of diversity and endemism, including anostracans (Eng et al., 1990) and are similar in community structure to other temporary aquatic habitats worldwide (King et al., 1996; Blaustein & Schwartz, 2001; De Meester et al., 2005; Williams, 2006; Zacharias & Zamparas, 2010; Boix et al., 2016; Jeffries et al., 2016).

In addition to the order Anostraca, vernal pools support a diverse assemblage of other large branchiopods, such as tadpole shrimp (Notostraca), clam shrimp (Spinicaudata), and water fleas (Cladocera) (King et al., 1996; Boix et al., 2016). Like Anostraca, all these groups produce resting eggs (Brendonck, 1996; Innes, 1997; Schönbrunner & Eder, 2006) and many are endemic to California vernal pools (Eng et al., 1990; King et al., 1996). Branchinecta lynchi ( Eng, Belk, Eriksen, 1990), the vernal pool fairy shrimp, is a species found in California and southern Oregon, and is currently listed as federally endangered (USFWS, 1996). This species is adapted to reach maturity and reproduce faster than other vernal pool branchiopods (Gallagher, 1996; Helm, 1998). Linderiella occidentalis (Dodds, 1923), the California fairy shrimp, is another common anostracan that often shares its environment with Branchinecta lynchi, though it usually requires a longer hydroperiod (Gallagher, 1996). This endemic species has not been listed as threatened or endangered (USFWS, 1996), though threats to its populations have been identified (Leyse et al., 2004). Notostraca and Spinicaudata species are also endemic to California vernal pools, including Lepidurus packardi (Simon, 1886) and Cyzicus californicus (Packard, 1883), respectively. Both species have longer life cycles than the anostracans (Helm, 1998) and have also been found to disrupt the sediment (bioturbation) during the aquatic phase (Croel & Kneitel, 2011). Lepidurus packardi, the vernal pool tadpole shrimp, is an endangered species (USFWS, 1996) that has been shown to be important in influencing ecosystem-level characteristics of vernal pools (Croel & Kneitel, 2011). However, the ecology of Cyzicus californicus, the California clam shrimp, has not been well studied (but see Eriksen & Brown, 1980; Helm, 1998).

The purpose of this study was to evaluate the effects of hydroperiod stability, thatch, and nutrients on the emergence and densities of endemic large branchiopods of California vernal pools. Hydroperiod is the preeminent factor influencing temporary aquatic ecosystems (Wellborn et al., 1996; Batzer, 2013), but less is known about species’ responses to hydroperiod stability in experimental settings (Kneitel, 2014). Plant thatch represents the previous terrestrial phase’s influence on the aquatic phase following inundation, and to the best of our knowledge, no study has addressed the potential for thatch to affect large branchiopods. Lastly, nutrients represent spatial subsidies that can occur with runoff from surrounding habitat matrix and can affect bottom-up control of the community. We conducted a full factorial experiment using mesocosms at the arboretum of the California State University, Sacramento campus. Mesocosms were lined with vernal pool soil to evaluate densities of Anostraca (Branhinecta lynchi and Linderiella occidentalis), Notostraca (Lepidurus packardi), and Spinicaudata (Cyzicus californicus) in response to treatments and how they correlated with water quality measurements (dissolved oxygen, conductivity, turbidity, phosphates, nitrates, and chlorophyll-a).

Methods

Experimental design

Soil from vernal pool complexes in the Elder Creek Watershed and Gill Ranch (Sacramento County, CA) were used for the mesocosm experiment (Kneitel & Lessin, 2010; Croel & Kneitel, 2011; Kneitel, 2014; Anderson & Kneitel, 2015). The top 6 cm of soil was removed to insure the presence of the invertebrate egg banks (Brendonck & De Meester, 2003). Soil was homogenized with a cement mixer to intersperse the egg bank.

In December 2014, 48 mesocosms (containers held 151 l; mesocosm dimensions: length = 1.03, width = 0.36 m, height = 0.72 m, area = 0.37 m2) were established outdoors at the California State University, Sacramento arboretum. Approximately 7 kg of the homogenized soil was added, which resulted in approximately 2 cm depth of soil. Mesocosms were left uncovered over the course of the study to allow for active dispersers to colonize. Well water was used to supplement natural rainfall to fill the mesocosms.

Twelve treatments were randomly assigned to mesocosms in a randomized block (n = 4 blocks) arrangement. The experimental design was a full factorial 2 × 2 × 3 that consisted of hydroperiod (stable and unstable), nutrient addition (control and addition), and thatch (control, native plant thatch, and exotic plant thatch). The stable-hydroperiod (long hydroperiod) treatment was inundated for 20 weeks (December–May) and the unstable-hydroperiod treatment consisted of a 9-week inundation (December–March), which desiccated and kept dry for 2 weeks, then refilled for another 9 weeks of inundation (March–May). Desiccation occurred naturally, and approximately 20 l was removed twice weekly over the last 2 weeks of the unstable hydroperiod. Removed water was poured through a net (0.2 mm mesh) and all filtered individuals were returned to the mesocosm. To ensure that the water removal did not create an added disturbance, the long hydroperiod treatments had the same procedure applied to them, but water was added to refill the mesocosm.

Nutrient addition treatments included nitrogen and phosphorus addition via an aqueous solution of NaNO3 and KH2PO4. A 0.5 mg/l concentration in a 48 ml solution was used for both N and P and added every two weeks. Plant thatch treatments included control, exotic plants, and native plants. Aboveground plant vegetation was collected from Mather Field (Sacramento County, CA) from vernal pools and adjacent upland habitat. Plants were haphazardly collected and included typical native and exotic plants from vernal pools. Native species included Eleocharis macrostachya Britton, Eryngium castrense Jepson, and Plagiobothrys stipitatus (Greene) I.M. Johnst., and exotics included Erodium botrys (Cav.) Bertol., Avena spp, and Hordeum spp. Fifty grams (dry weight) of vegetation were added to the appropriate treatment replicates prior to inundation.

The large branchiopods (Branchinecta lynchi, Linderiella occidentalis, Lepidurus packardi, and Cyzicus californicus) were sampled by gently sweeping an aquarium net (dimension = 17.8 × 25.4 cm, mesh size = 0.2 mm) for 10 s in a circular fashion over the whole area and depth of the mesocosms. To ensure that the presence of thatch did not inhibit invertebrate sampling, another 5-s sweep focused on the thatch was conducted. Captured individuals were washed into a tray for enumeration and returned to the mesocosm. Invertebrate communities were sampled in each mesocosm at weeks 3, 5, 7, and 9 (short-early and long hydroperiod), and then at weeks 14, 16, 18, and 20 (short-late and long hydroperiod). Water quality characteristics were measured that included turbidity (NTU; with LaMotte 2020i turbidity meter), conductivity (μS; with Oakton pH/CON 300 m), dissolved oxygen (mg/l; with Oakton pH/DO 300 m), orthophosphates (PO43− mg/l; with Hach DR2800 spectrophotometer), and nitrates (NO3–N mg/l; with Hach DR2800 spectrophotometer). Chlorophyll-a (μg/l) in vivo measures were conducted with a Trilogy Laboratory Fluorometer. Conductivity and dissolved oxygen were measured on the same day as the invertebrates (prior to sampling). A 50-ml sample was taken from each mesocosm and brought to the Kneitel lab for sampling the remaining variables within several days.

Statistical analysis

To assess the effects of treatments on each of the species’ densities, 3-way repeated measures MANOVA was used with hydroperiod, thatch addition, and nutrient addition as independent variables. All densities were ln-transformed to correct for distributions, but sphericity and normality assumptions were violated, and therefore the Greenhouse-Geisser correction was used. Bonferroni-corrected post hoc analyses were conducted with significant thatch effects to assess differences among the 3 treatments. A similar 3-way repeated measures MANOVA was also used to assess measured water variables (Chlorophyll-a, dissolved oxygen, conductivity, turbidity, phosphates, and nitrates). Correlations among water physical and chemical variables and species densities were assessed using data from Week 14 because all species were present and it captured both stable and unstable-hydroperiod treatments. Statistical tests were conducted using IBM SPSS, version 24 (IBM Corp., Armonk, NY, USA).

Results

Species responses to treatments were variable, but broad patterns were found related to taxonomic groups. Anostracans (Branchinecta lynchi and Linderiella occidentalis) emerged earlier and dominated during the early season than Lepidurus packardi and Cyzicus californicus. All species densities exhibited unimodal patterns over time. Some species densities were weakly correlated with each other. Branchinecta lynchi was positively correlated with L. occidentalis (r = 0.29, P = 0.045) and negatively correlated with C. californicus (r = −0.43, P = 0.002). Lepidurus packardi was positively correlated with C. californicus (r = 0.47, P = 0.001).

The multivariate effects of time, time x hydroperiod, and time x thatch were significant (Table 1A). All species emergence and population densities changed over time, and all species but L. occidentalis were affected by hydroperiod stability. Branchinecta lynchi had overall higher densities in the unstable hydroperiod since refilling allowed another cohort to emerge (Fig. 1a). In contrast, L. packardi and C. californicus had higher densities in the stable hydroperiod since they emerged later and require a longer hydroperiod for their life cycle (Fig. 1c, d). All species but C. californicus responded to the thatch treatments. Both native and exotic thatch reduced B. lynchi and L. occidentalis densities, but native and exotic thatch were not significantly different from each other (Fig. 1a). L. packardi densities were significantly reduced by both thatch types, and native thatch significantly reduced densities compared to exotic plant thatch (Fig. 1c).
Table 1

Repeated measures MANOVA results (full model and individual dependent variables) for (A) focal species’ densities and (B) water quality variables

A. Biotic variables

Independent variables

Full model

Branchinecta lynchi

Linderiella occidentalis

Lepidurus packardi

Cyzicus californicus

Wilks’ λ

P

F

P

F

P

F

P

F

P

Time (T)

0.045

<0.001

14.49

<0.001

267.59

<0.001

29.81

<0.001

78.96

<0.001

T × Hydroperiod (H)

0.511

<0.001

2.47

0.04

0.83

0.62

2.60

0.008

55.44

<0.001

T × Thatch (Th)

0.477

<0.001

10.16

<0.001

12.15

<0.001

4.44

0.003

6.47

0.17

T × Nutrient (N)

0.883

0.29

0.43

0.78

3.00

0.09

0.60

0.41

1.37

0.69

T × H × Th

0.804

0.48

1.25

0.74

2.25

0.56

2.64

0.06

2.72

0.80

T × H × N

0.930

0. 92

0.90

0.45

0.28

0.90

0.37

0.62

2.12

0.45

T × Th × N

0.849

0.92

1.76

0.51

2.31

0.55

1.10

0.50

1.18

0.99

T × H × Th × N

0.805

0.49

3.10

0.12

1.62

0.74

1.39

0.35

2.44

0.74

B. Water quality variables

Independent variables

Full model

Chlorophyll-a

Dissolved oxygen

Conductivity

Wilks’ λ

P

F

P

F

P

F

P

Time (T)

0.018

<0.001

22.92

<0.001

299.01

<0.001

20.85

<0.001

T × Hydroperiod (H)

0.407

<0.001

1.99

0.11

5.56

0.008

1.54

0.22

T × Thatch (Th)

0.506

<0.001

1.44

0.20

4.50

0.004

1.17

0.32

T × Nutrient (N)

0.818

0.169

2.51

0.05

0.35

0.67

1.39

0.25

T × H × Th

0.735

0.648

0.74

0.64

0.32

0.84

0.89

0.43

T × H × N

0. 905

0. 982

0.53

0.69

0.17

0.82

0.64

0.44

T × Th × N

0.782

0.959

0.88

0.53

0.23

0.90

0.83

0.45

T × H × Th × N

0.803

0.992

0.40

0.90

0.34

0.83

1.12

0.34

B. Water variables (continued)

Independent variables

Turbidity

Phosphate

Nitrate

F

P

F

P

F

P

Time (T)

36.99

<0.001

37.79

<0.001

25.67

<0.001

T × Hydroperiod (H)

29.62

<0.001

2.49

0.07

0.24

0.92

T × Thatch (Th)

1.97

0.10

0.65

0.68

2.28

0.02

T × Nutrient (N)

0.22

0.82

2.83

0.05

0.68

0.62

T × H × Th

2.05

0.09

0.68

0.66

0.61

0.78

T × H × N

0. 18

0. 86

0.89

0.44

1.08

0.38

T × Th × N

0.95

0.45

0.74

0.61

0.86

0.56

T × H × Th × N

0.91

0.47

0.41

0.86

0.75

0.65

T time, H hydroperiod, Th thatch, N nutrients

Fig. 1

Plots of aBranchinecta lynchi, bLinderiella occidentalis, cLepidurus packardi, and dCyzicus californicus densities over time in hydroperiod and plant thatch treatments. Note: y-axes on different scales

The MANOVA full model for the water variables were significant for time, time x hydroperiod, and time x thatch (Table 1B). Both dissolved oxygen and turbidity were significantly reduced by an unstable hydroperiod. Thatch addition significantly reduced dissolved oxygen and nitrates. Lastly, nutrient addition significantly increased both chlorophyll-a and phosphates (Table 1B).

During Week 14, many of the water variables correlated with all the species. Dissolved oxygen was positively correlated with B. lynchi (r = 0.55, P < 0.001) and negatively correlated with L. packardi (r = −0.29, P = 0.04) and C. californicus (r = −0.71, P < 0.001). Conductivity was negatively correlated with B. lynchi (r = −0.40, P = 0.004) and L. occidentalis (r = −0.47, P = 0.001). Turbidity was positively correlated with both L. packardi (r = 0.45, P = 0.002) and C. californicus (r = 0.80, P < 0.001). Chlorophyll-a was positively correlated with each of the species: B. lynchi (r = 0.33, P = 0.021), L. occidentalis (r = 0.34, P = 0.020), L. packardi (r = 0.30, P = 0.037), and C. californicus (r = 0.34, P = 0.020).

Discussion

Species responses to treatments changed over time: anostracans (Branchinecta lynchi and Linderiella occidentalis) were most dense during the early part of the hydroperiod, whereas Lepidurus packardi and Cyzicus californicus tended to be more abundant during the latter part of the hydroperiod. Hydroperiod stability and thatch directly affected most of the populations, but interactions among treatments were not found.

Hydroperiod stability, which is often identified as a cornerstone factor in temporary pond ecology (Schneider & Frost, 1996; Wellborn et al., 1996; DeMeester et al., 2005; Williams, 2006; Vanschoenwinkel et al., 2010b, 2013; Batzer, 2013; Brendonck et al., 2015; O’Neill, 2016) had effects on all species except for L. occidentalis. The hydroperiod effects were, however, different among species based on life history characteristics, as previously observed (Schneider & Frost, 1996; Wellborn et al., 1996). The anostracans had higher densities in the unstable compared to stable hydroperiod treatments. Branchinecta lynchi and L. occidentalis tend to emerge from resting eggs more quickly and have shorter life cycles (Helm, 1998). They had already completed their life cycle in the long hydroperiod treatments by mid-experiment, whereas they re-emerged in the unstable-hydroperiod treatments that refilled. In contrast, L. packardi and C. californicus, which emerge later and have longer life cycles (Helm, 1998), had higher densities in the long hydroperiod treatments. Other temporary pond crustaceans increased abundance in longer hydroperiods (Holland & Jenkins, 1998; Porst et al., 2012), by allowing populations to increase in size or populations with longer life cycles to persist in the community (Schneider & Frost, 1996). In the present study, the timing of emergence and the life cycle length relative to the hydroperiod length determined these patterns. Similar patterns have been found in other temporary aquatic ecosystems (Wiggins et al., 1980; Brooks, 2000; Larned et al., 2010; Bogan & Lytle, 2011; Ruhí et al., 2013; Stubbington et al., 2016), and highlights how environmental variation can interact with species life histories to influence spatial and temporal patterns of population in seasonal ecosystems.

Plant thatch addition (native and exotic species) had strong negative effects on each of the species, except C. californicus. Temporary aquatic ecosystems would have thatch present as a legacy from the previous terrestrial phase, indicating a novel effect on large branchiopod ecology. These effects may have been due to thatch acting as inhibitory structure or indirectly through changes in water chemistry with decomposition. One likely explanation is the thatch layer attenuated light and thereby inhibited invertebrate emergence from the resting stage. Previous studies with Anostraca and Notostraca have found decreased emergence from their resting stages with decreased light (e.g., Horiguchi et al., 2009; Kashiyama et al., 2010; Pinceel et al., 2013). Plant thatch can reduce light penetration (Facelli & Pickett, 1991) and therefore there is the potential to reduce light cues to resting eggs. Previous studies have also identified negative relationships between thatch and invertebrate densities, which have also been explained by changes in water chemistry (e.g., Christensen & Crumpton, 2010).

Decomposition of plant matter might be one reason for the effects of thatch on water chemistry, as plant decomposition supports microbial life (Webster & Benfield, 1986). In the first few weeks of inundation, decomposition of aquatic plant matter proceeds rapidly (Belova, 1993), which would fit the observed decrease in dissolved oxygen associated with rapid bacterial growth. Brendonck (1996) found a negative relationship between dissolved oxygen and hatching of selected branchiopods. Thus, lower dissolved oxygen resulting from decomposition might be partly responsible for the strong effect of thatch on species emergence in this experiment. Unmeasured variables, including temperature, salinity, or pH, may have also contributed to decreased densities directly (e.g., Waterkeyn et al., 2009) or modified species interactions (e.g., Ewald et al., 2013).

Another potential explanation for the effects of thatch is the modification of species interactions. It is possible that thatch increased competition or predator–prey interactions in the mesocosms, such that densities were reduced. For example, Triops (Notostraca) is well known to have negative top-down effects on other crustaceans of temporary ponds (Boix et al., 2006; Waterkeyn et al., 2011, 2016). Further, bioturbation caused by L. packardi may have also indirectly reduced species (Yee et al., 2005; Waterkeyn et al., 2011, 2016) in the latter part of the hydroperiod. These explanations are not likely, however, since negative relationships were not found between L. packardi and the other species or between turbidity and the other species. In fact, previous studies have found that habitat structure has increased species abundance and richness because it increases heterogeneity, while reducing competition and predator–prey interactions (e.g., van Donk & van de Bund, 2002; St. Pierre & Kovalenko, 2014; Stein et al., 2014). Therefore, thatch addition most likely inhibited species emergence directly with light cues or water chemistry.

Nutrient addition had no direct effects on species densities, but all species were positively correlated with chlorophyll-a concentrations, which were positively affected by nutrient addition. The positive relationship likely resulted from bottom-up effects (effects of nutrients on higher trophic levels), a pattern observed in many other aquatic ecosystems (e.g., Batzer & Resh, 1991; Balla & Davis, 1995; Yee et al., 2007). Bottom-up effects, however, can also be mediated by the number of trophic levels present in the community (Hansson, 1992; Power, 1992; Kneitel & Miller, 2002; Waterkeyn et al., 2011). For example, the top-down effects (effects of predators on lower trophic levels) could have resulted from the large branchiopods reducing micro-crustaceans and therefore positively affecting the lowest trophic level, a trophic cascade (Power, 1992; Waterkeyn et al., 2011, 2016).

As found in the present study, many water variables have also been implicated as factors in temporary pond community assembly, including conductivity (King et al., 1996; Waterkeyn et al., 2009; Vanschoenwinkel et al., 2010a; Florencio et al., 2014) and dissolved oxygen (Moore & Burn, 1968; Smith et al., 2003). Turbidity is also important in some temporary pond ecosystems because of the presence of certain species being bioturbators, whose actions result in suspended sediment in the water column (Yee et al., 2005; Croel & Kneitel, 2011; Waterkeyn et al., 2016) and can influence water chemistry and nutrient cycling (Covich et al., 1999). We found similar turbidity patterns in the present study with the presence of both L. packardi, and C. californicus.

Alternative explanations may also explain some of the patterns or variation found in this study. First, the relative densities of resting eggs in the soil were unknown, but could have influenced the relative densities of species in the mesocosms. However, since the soil was homogenized prior to the experiment, it is unlikely that this influenced treatment responses. Second, the behavior of C. californicus and L. packardi as bottom dwellers could have influenced their detection in the mesocosms, especially in thatch treatments. However, our sampling methodology included sweeps along the mesocosm bottom without disrupting the soil, and treatments with thatch were sampled for additional time in the thatch to ensure capture of bottom-dwelling invertebrates. We believe these possible explanations were unlikely explanations for general patterns, but could have explained some of the variation.

Hydroperiod stability had strong effects on each of the species, except L. occidentalis. The other treatment effects, however, highlight novel and understudied aspects of temporary pond ecology and by extension endemic large branchiopods. The thatch and nutrient addition represent temporal and spatial linkages, respectively, to the local community. The thatch treatments represent the previous terrestrial phase prior to inundation. Most studies focus on a single or multiple years of inundation cycle to understand populations. However, these results suggest that increased thatch and thatch type (native versus exotic plants) during the terrestrial phase can inhibit these endemic branchiopods. Because of the inhibitory effects of thatch, the previous dry phase needs to be considered, including the factors affecting vegetation cover and composition (Bliss & Zedler, 1998; Javornik & Collinge, 2016; Rocarpin et al., 2016).

Conclusions

Many large branchiopods, an understudied group of invertebrates, are endemic to temporary waters (Brendonck, 1996; Boix et al., 2016), including California vernal pools (King et al., 1996; Kneitel, 2016). Large branchiopods, such as the ones in the present study, are flagship species of many seasonal freshwater habitats (Brendonck et al., 2008; Boix et al., 2016). Our understanding of many species’ ecology is still in its infancy, especially in these ecosystems. Our study found that the emergence and population sizes of 4 endemics of California vernal pools were affected by hydroperiod stability, thatch, and indirectly by nutrients. There were species-specific patterns in response to hydroperiod stability, but most species were negatively affected by thatch and positively affected by nutrients.

An understanding of these threatened and endangered species under different ecological conditions will facilitate management under changing environmental conditions. Two of the species, Branchinecta lynchi and Lepidurus packardi, are federally-listed endangered and therefore these results have implications for their management. For example, reductions in aboveground thatch levels by way of moderate grazing (e.g., Marty, 2005) and restoration that enhances variation in hydro-regime (e.g., Ruhí et al., 2016) may greatly benefit their populations. Future work could examine other ecological factors influencing large branchiopod populations, including biotic interactions. The importance of temporary freshwater ecosystems, including California vernal pools, extend from the species level to the community and ecosystem level (Duffy & Kahara, 2011) and therefore their conservation and management is critical for biodiversity and functioning (Dudgeon et al., 2006; Batzer, 2013; Van den Broeck et al., 2015; Biggs et al., 2016).

Notes

Acknowledgements

We gratefully acknowledge others who assisted on this project: Trisha Velasquez, Nabilah Fareed, Adam Kneitel, and Nina Kneitel. We also appreciate Dr. Mike Baad’s continued support at the CSUS Arboretum and reviewers’ comments that improved the manuscript. This research was supported by a National Science Foundation grant DEB 1354724 and sampled under USFWS Permit TE192702 to JMK.

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© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Department of Biological SciencesCalifornia State University, SacramentoSacramentoUSA
  2. 2.Department of Environmental StudiesCalifornia State University, SacramentoSacramentoUSA

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