Introduction

Fens and wet meadows are high diversity wetland habitats that are common in the mountain environment (Klikoff, 1965; Benedict and Major, 1982; Benedict, 1983; Bedford and Godwin, 2003). Fen peatlands are perennially saturated with water, whereas wet meadows are saturated with water during only part of the year and have mineral soils (Williams, 2006; Mitsch and Gosselink, 2007). The hydrology, soil characteristics, and flora of these habitats are well understood and are used in wetland classification schemes (Mitsch and Gosselink, 2007), but the distribution and abundance of invertebrate assemblages of mountain wetlands have received comparatively little attention (Wissinger et al., 1999). Further, although wetlands are often described as an aquatic-terrestrial ecotone (Batzer and Wissinger, 1996), aquatic and terrestrial fauna are rarely investigated simultaneously in these mountain wetlands.

Work to date in high elevation and/or high latitude environments suggests the importance of invertebrates in these wetlands. Finnamore (1994) for instance found that arthropods represented 77% of terrestrial taxa in an Alberta fen and related habitats, versus 16% and 6% for plant and vertebrate taxa, respectively (see also Keiper et al., 2002; Spitzer and Danks, 2006; Savage et al., 2011). Simonson et al. (2001) found montane wet meadows to have disproportionately high butterfly diversity, despite accounting for a small proportion of the landscape. Studies in both North America and Europe have shown that invertebrate densities in these habitats can drive avian wetland use, size and spacing of territories, and breeding success (Orians, 1966; Rolando et al., 2007). Most work on aquatic invertebrates in peatlands has centered on permanent pond habitats versus shallower, ephemeral habitats with dense emergent vegetation (Batzer and Wissinger, 1996). Ephemeral mountain waters can have lower richness and abundance than permanent water bodies (Duffy, 1999; Wissinger et al., 1999; Euliss et al., 2004), and trophic complexity generally increases with increasing habitat permanence (Batzer and Wissinger, 1996; Duffy, 1999; Schneider, 1999). Temporary wetland pools nonetheless can support high abundances of chironomids, caddisflies, and dytiscid beetles, and chironomid species richness can be high in these habitats (Wiggins et al., 1980; Batzer and Wissinger, 1996; Wissinger et al., 1999). Detrital decomposition during waterless phases may make this food resource more available to fauna with resulting high insect productivity in ephemeral waters (Wiggins et al., 1980; Batzer and Wissinger, 1996). Insects are sensitive to subtle flow differences (Schowalter, 2006), and even low (<1 cm sec⁻¹) sheet flows (Heinselman, 1970; Kadlec, 1990) in ephemerally inundated fens and wet meadows may be important in determining population densities of some taxa.

We examined three questions in the Sierra Nevada mountains of California, U.S.A.: (1) What are the estimated relative contributions of terrestrial (epigeal) and aquatic invertebrates to diversity and abundance in these wetlands, as information on relative diversity of habitats is critical to management decisions (Tierney et al., 2009; Hobbs et al., 2010; Thompson et al., 2011)? (2) Do aquatic and terrestrial invertebrate assemblages differ as a function of wetland type (fen versus wet meadow)? (3) To what extent do aquatic assemblages differ as a function of presence or absence of slow sheet flow across these wetlands? This initial study of Sierra Nevada wetland assemblages had a unique combination of elements: (1) a large, almost pristine, and remote study landscape of 6200 km² (Yosemite, Sequoia, and Kings Canyon National Parks); (2) extensive sampling (80 backcountry sites) at elevations as high as 3700 m; (3) simultaneous examination of aquatic and terrestrial assemblages; (4) analysis of all arthropod taxa rather than a subset of targeted groups; and (5) a focus on vernal waters versus permanent ponds or marshes.

Methods

We contrasted assemblage structure of the aquatic benthos using a 2 × 2 design (Wetland: Fen, Wet meadow; Flow: Absent, Present). Epigeal terrestrial invertebrates were compared as a function of wetland type (1 × 2). We did not sample infauna or soil fauna. We contrasted terrestrial and aquatic assemblages using a 2 × 2 design (Habitat: Aquatic, Terrestrial; Wetland: Fen, Wet meadow) for area-independent metrics (e.g., expected number of species), because samples were necessarily collected with different sampling techniques: standard sweep (cone) netting for terrestrial fauna and standard sweep (D-frame) netting for aquatic fauna. Area-dependent metrics (e.g., species richness) were not compared across habitats. The study was one component of a wetland “vital signs” program coordinated by the National Park Service (NPS; Davis, 2005; Fancy et al., 2009; Tierney et al., 2009). The goal was to address the questions outlined above at a large number of sites, each visited once, distributed across the sizeable landscape of three national parks, over a comparatively short period of time (two growing seasons).

Results

We identified 14,805 wetland invertebrates from terrestrial and aquatic habitat. Terrestrial samples included 147 families, and aquatic samples yielded 48 families (Appendix 1). Sixty-seven percent of terrestrial families occurred in three or more samples, versus 60% for aquatic families. Rank abundance plots for terrestrial and aquatic faunas approximated a log normal distribution and log series, respectively; high dominance is apparent in the latter (Fig. 1). Although curves were almost congruent for each assemblage across wetland types within a given assemblage, there was slightly more abundance at mid-range family ranks for fen fauna in both terrestrial and aquatic assemblages, and there were more total families in wet meadow than in fen habitat for both terrestrial (134 versus 117) and aquatic (44 versus 37) fauna (Fig. 1, Appendix 1). Sampling terrestrial and aquatic habitat required different methodologies, but assemblage level comparisons across faunas were possible for metrics that were proportion based or had compensation for differing sample sizes (Table 1). Terrestrial fauna clearly contributed the majority of the total arthropod diversity present in these fens and wet meadows, as all assemblage contrasts were highly significant. Rarefied terrestrial family and morphospecies richnesses were 10–20% higher than those of the aquatic habitats, and associated variance was low (Table 1). Terrestrial evenness was up to twice that of the aquatics as indicated by Hurlbert's PIE, and terrestrial faunas had about half the dominance of the aquatics as assessed at both the family and morphospecies levels. Predators made up a higher proportion of the terrestrial assemblage, but there was a significant interaction term (Table 1). When terrestrial and aquatic assemblages were examined in combination, there were significant differences as a function of wetland type only for the two PIE metrics, but there was a significant trend of greater diversity in fens than wet meadows when all metrics were considered (P < 0.0025).

FIGURE 1

Rank abundance plot for families comparing terrestrial and aquatic faunas as a function of wetland type, based on mean abundances for study.

TABLE 1

Means, standard errors, and results of 2 × 2 ANOVAs (n  =  133; df  =  1,1,1,130) comparing terrestrial versus aquatic faunas (Assemblage) and as a function of wetland type (Habitat). * and ** flag P-values less than 0.05 before and after, respectively, sequential Bonferroni correction across all assemblage metrics. See Methods for further metric description.

When terrestrial fauna were considered in isolation for all assemblage metrics, there were additional significant differences as a function of wetland type (one-tailed, independent t-tests; fen n  =  33, wet meadow n  =  47, df  =  78). There was greater abundance in fens (  =  178 individuals/50-sweep sample, SE  =  20.4) than in wet meadows (  =  137, SE  =  25). Morphospecies richness per sample was also higher in fens (  =  38.1, SE  =  3.63) than in wet meadows (  =  29.0, SE  =  2.51), as was morphospecies PIE (Table 1). There was a higher proportion of predators in wet meadows (Table 1). Several other metrics were consistent with the trend of higher diversity in fens, and had low (P < 0.15), but not significant, P values (family richness, E(S), species dominance, and family PIE), and there was again a significant overall trend of higher diversity in fens (P < 0.025).

The terrestrial fauna was dominated by Diptera, in terms of family richness (43), abundance (mean  =  70/50-sweep sample), and frequency of occurrence (1.0, Table 2, Appendix 1). Hymenoptera (28 families), Coleoptera (24), and Hemiptera (19) were also diverse. Cicadellid leafhoppers had the greatest morphospecies richness. Other abundant groups included Hemiptera and Araneae (Table 2, Appendix 1). Only Diptera were found in each sample, but Hemiptera, Araneae, and Hymenoptera all had frequencies of ∼0.8. Cicadellids had the greatest overall family abundance (mean  =  20/sample), followed by another hemipteran family (Aphididae, 15/sample), thomisid crab spiders, and chloropid, drosophilid, and anthomyiid flies (all ∼12/sample, Table 2, Appendix 1). Cicadellids, thomisids, and muscid and anthomyiid flies had the highest frequencies of occurrence. Less than 1% of the terrestrial fauna was composed of taxa with early aquatic life stages. The proportion of such taxa was positively and significantly related to meadow area, although the proportion of the variance explained was small (linear regression, P  =  0.016, R²  =  0.064, df  =  1,79).

TABLE 2

Mean relative abundance (number of individuals/50 sweeps), standard errors, frequency of occurrence across all samples, and results of one-tailed, independent t-tests (fen n  =  33, wet meadow n  =  47, df  =  78) comparing terrestrial orders, plus Acari, and the 10 most abundant families as a function of wetland type. Psocoptera lacked sufficient abundance for testing. * and ** flag P-values less than 0.05 before and after, respectively, sequential Bonferroni correction for all taxa within a given order.

There were a number of terrestrial population differences as a function of wetland type (Table 2, Appendix 1). The two most abundant families in wet meadows, Aphididae and Drosophilidae, were not among the 10 most abundant families in fens, although the rest of the dominant families were broadly similar in rank between the two wetland types. Cicadellids, Lepidoptera, Diptera, anthomyiid, muscid, chloropid, and ephydrid flies, and thomisids were all significantly more abundant in fens than in wet meadows. Only mirid leaf bugs were significantly more abundant in wet meadows than fens, and there was an overall trend of higher population abundances in fens (P < 0.05). Frequencies of the most common fauna were similar across habitats. Fens and wet meadow had 105 families in common and 12 and 29 families unique to fens and wet meadows, respectively (Appendix 1). The Sørensen quantitative similarity index for these two assemblages was 0.63.

Cluster analysis of terrestrial sampling sites showed separation of some wet meadows from other locations (Appendix 2). A low MRPP P-value (0.0012, randomization test) suggests that fens and wet meadows were compositionally distinct, but the low within-group agreement value, or effect size (A  =  0.030), indicates a substantial variation within each habitat type. A second MRPP using the new group membership variable generated from cluster analysis resulted in a lower P value (<0.0001) and higher A ( = 0.18), underscoring the potential importance of other factors in addition to wetland type; some of the new groupings had a latitudinal component. Ordination via NMS showed some separation of sites by habitat type, particularly along Axis 1 (Fig. 2). The ordination suggests that the two habitat types were not strongly compositionally distinct, but there was less within-group variation in ordinal space for fens than wet meadows. The explanatory variables canopy height (R²  =  0.31), elevation (R²  =  0.34), and ordinal day (R²  =  0.28) were most strongly associated with Axis 1 (Fig. 2).

FIGURE 2

Ordination (joint) plots of terrestrial assemblage structure across sites in two-dimensional space using nonmetric multidimensional scaling. Distance between site icons approximates dissimilarity between sites; convex hulls surround sites of a given habitat type. Plots are scaled by proportion of maximum; orthogonality was 100% for each axis pairing. Axis labels include R² values estimating post-hoc percent of variation within the distance matrix that is explained by each axis. Cumulative R² was 0.54. Explanatory variables in joint plot: C  =  canopy height, E  =  elevation, O  =  ordinal day. Minimum explanatory variable-axis correlation for inclusion in the joint plot was R²  =  0.20.

Aquatic fauna examined in isolation for all assemblage metrics showed notably few significant differences as a function of either wetland type or flow (Table 3). There was a higher proportion of predators in fens, and there was a higher proportion of Ephemeroptera, Plecoptera, and Trichoptera (%EPT) in sites with sheet flow. There were significant trends across all metrics for overall higher diversity in flow and in fens (P < 0.001 and P < 0.025, respectively), despite greater absolute family richness in wet meadows.

TABLE 3

Means, standard errors, and results of 2 × 2 ANOVAs (n  =  52; df  =  1,1,1,48) comparing aquatic fauna as a function of wetland type and water flow. Metrics are based on 5 m sweep samples. * and ** flag P-values less than 0.05 before and after, respectively, sequential Bonferroni correction across all assemblage metrics. See Methods for further metric description.

The aquatic fauna, like the terrestrials, was dominated by Diptera in terms of family richness (12) and frequency of occurrence (0.94), but Diptera were second to clams (Veneroida) in terms of abundance (50 versus 78/sample; Table 4, Appendix 1). Family richnesses of other groups were well below Diptera: Acari (6), Ephemeroptera (6), Trichoptera (5), and Odonata (5), and abundances of these groups were far below those of Diptera and Veneroida (Table 4). Chironomids had the highest morphospecies richness. Beetles, clams, and mites followed Diptera in frequency and were the only taxa with frequencies above 0.5. Sphaeriid clams and chironomids were by far the most abundant families (Table 4, Appendix 1).

TABLE 4

Mean relative abundance (number of individuals/5 m sweep), standard errors, frequency of occurrence across all samples, and results of 2 × 2 ANOVAs (n  =  52; df  =  1,1,1,48) comparing aquatic orders, plus Acari, and the 10 most abundant families as a function of wetland type and water flow. WM  =  wet meadow; * and ** flag P-values less than 0.05 before and after, respectively, sequential Bonferroni correction for all taxa within a given order.

There were comparatively few differences for aquatic assemblage metrics as a function of habitat and flow, but a number of population differences were apparent (Table 4, Appendix 1). Although clams and chironomids were the most abundant families in both wetland types, mosquitos, flatworms, and ephemerellid mayflies were abundant in wet meadows but not fens (ephemerellids were absent), and coenagrionid damselflies were abundant in fens but were almost absent in wet meadows. Variance among samples was high, and there were significant differences as a function of wetland type for Diptera and Culicidae only (more abundant in wet meadows). Clams and chironomids were the two most abundant taxa both with or without flow. Mosquitos and damselflies were abundant in no-flow habitats, but almost absent if even very slow sheet flow was present. Flatworms and ephemerellids were common with flow, but absent from still water. There were more significant population differences as a function of flow than for wetland type: Plecoptera, chloroperlid stoneflies, mites, clams, and flatworms were all significantly more abundant in flow, and Hemiptera, Diptera, and mosquitos were significantly more abundant in quiescent water. There were significant interaction terms for mosquitos and dysticid predaceous diving beetles. Although individual taxa had different abundances as a function of wetland type or water flow, there was not an overall directional trend for either factor across all taxa (P > 0.25 for both factors). Frequencies of the most common fauna were relatively similar across habitats, but mites occurred about 50% more frequently in fens than wet meadows. Fens and wet meadow had 33 families in common and only 4 and 11 families unique to fens and wet meadows, respectively (Appendix 1). The Sørensen quantitative similarity index for aquatic assemblages was 0.66. In contrast, there were only 22 families common to aquatic habitats across flow regimes but 9 families found only where flow was absent and 17 found only where flow was present (Appendix 1). In turn, the similarity index for no-flow and flow assemblages was 0.34—about half that of either the terrestrial or aquatic wetland assemblage similarities.

There was some clustering of aquatic sites as a function of flow regime; in particular, a number of wet meadow sites with flow showed higher level separation from other sites (Appendix 3). As with terrestrial assemblages, MRPP suggested some relative similarity within habitat groups (P  =  0.031) but also high within-group variation (A  =  0.048). The MRPP based on the group membership variable from the cluster analysis again had a lower P value (<0.0001) and higher A (0.25). Some of the new cluster groupings suggested latitudinal differences. Ordination (NMS) plots showed more similarities than differences across habitat types, but some dissimilarity was observed for wet meadows with flow (Fig. 3). Aquatic explanatory variables were more weakly correlated with axes than in the terrestrial NMS. The strongest explanatory variable correlations were water depth with Axis 1 (R²  =  0.19) and elevation with Axis 3 (R²  =  0.16; Fig. 3).

FIGURE 3

Ordination (joint) plots of aquatic assemblage structure across sites in two-dimensional space using nonmetric multidimensional scaling. Cumulative R² was 0.42. Explanatory variables in joint plot: E  =  elevation, W  =  water depth. Minimum explanatory variable-axis correlation for inclusion in the joint plot was R²  =  0.15. See Figure 2 caption for additional information.

Discussion

The terrestrial assemblage accounted for most of the diversity in these wetlands and had more evenness and morphospecies richness as well as three times the family richness and half the dominance of the aquatic assemblage. The log normal distribution approximated by the terrestrial fauna in both fens and wet meadows also indicated high evenness (see also Savage et al., 2011) and typifies a large, mature, and varied assemblage, whereas the log series approximated by the aquatic fauna in both wetland types indicates a smaller number of abundant taxa (clams and midges in this study) and the dominance of one or a few factors in controlling an assemblage's ecology (Magurran, 2004). Hydroperiod is one such major determinant of aquatic diversity in mountain ponds (Duffy, 1999; Schneider, 1999; Wissinger et al., 1999; but see Batzer et al., 2004; Hanson et al., 2009), and the ephemeral waters that we investigated harbored a simpler assemblage than is found in more persistent waters and one that was lacking in vertebrates such as amphibians (Wissinger et al., 1999) and fishes (Zedler, 2003). Top predators were instead insects, such as diving beetles, damselflies, stoneflies, mites, and flatworms, as has been observed in other vernal and autumnal ponds (Wiggins et al., 1980; Batzer and Wissinger, 1996; Wissinger et al., 1999). Many of these predators were absent in our most ephemeral habitats, which were often dominated by chironomids and sphaeriid clams, and were only relatively diverse and abundant in the vernal ponds that persisted until mid-summer (see also Neldner and Pennak, 1955; Wiggins et al., 1980; Batzer and Wissinger, 1996).

Fens and wet meadows are ecotones that contain terrestrial and aquatic habitats that interdigitate in space and time as ephemeral ponds cyclically flood and dry (see also Haslett, 1997, 2001; Wettstein and Schmid, 1999). The aquatic fauna of ephemeral ponds often have relatively low diversity (Wissinger et al., 1999; Williams, 2006), but when aquatic diversity is combined with that of the terrestrial assemblage of these wetlands, this ecotonal environment has rather high overall diversity. Inclusion of terrestrial soil fauna and aquatic infauna would increase diversity still further.

It was striking that adult forms of taxa with the most abundant aquatic nymphs or larvae were almost absent from our terrestrial samples. Adult caddisflies, odonates, stoneflies, mosquitos, and chironomids accounted collectively for only 0.32% of total terrestrial individuals despite representing 38% of the aquatic assemblage. Adults of these taxa were similarly uncommon (2.7%) in the terrestrial assemblage examined by another study of Sierra wet meadows (Holmquist et al., 2010). Such taxa are frequently observed in upland habitats, so export from wetlands is at least a partial explanation for the discrepancy. The vernal ponds have less spatial extent than the rest of these wetlands, so these populations would necessarily be less dense upon emergence and dispersion in the terrestrial environment. The positive relationship between wetland area and presence of adult forms of aquatic taxa offers additional support to the possible influence of meso-scale landscape structure on boundary dynamics and ultimate retention of such fauna. More emigration would be expected from smaller patches (i.e., wetlands in the current study) with a larger perimeter:area ratio (Wiens et al., 1985; Ims, 1995) potentially resulting in lower proportions of adults of aquatic taxa. The wetland-upland interface should be a low contrast boundary with high permeability (Wiens et al., 1985; Stamps et al., 1987; Holmquist, 1998) for many terrestrial fauna, ultimately allowing high connectivity between wetlands and uplands. Indeed, Haslett (1997) and Wettstein and Schmid (1999) found significant numbers of upland fauna in subalpine wetland samples in the Austrian and Swiss Alps. In contrast to our current study, adult phases of aquatic insects can comprise 31% of terrestrial arthropod assemblages in desert wetlands (Holmquist et al., 2011) isolated in a xeric matrix (Tiner, 2003). This higher relative abundance of terrestrial adult phases of aquatic taxa at desert springs suggests fidelity of aquatic taxa that may be driven by the higher contrast boundaries encountered at the spring margins. We may also have missed some short adult phases in our fen and wet meadow sampling, and predation may account for some of the disparity as well. Interestingly, two less common dipterans, ceratopogonid biting midges and tipulid crane flies, were proportionally more abundant in our terrestrial mountain wetland samples than in the aquatic samples. It is possible that these midges have more fidelity to the wetland environment throughout their life cycles than do some of the more abundant groups.

Wetland type had an influence on invertebrates, particularly terrestrial fauna. The higher diversity and abundance of terrestrial fauna that we observed in fens may have been due to greater soil moisture and plant biomass relative to wet meadows; NMS ordination suggests that variation in canopy height may be an influence on wet meadow fauna in particular. In contrast, aquatic taxa of peatlands and other wetlands are often dominated by generalists that are widely distributed across wetland types (Danks and Rosenberg, 1987; Euliss et al., 1999).

The presence or absence of slow flow had more effect on aquatic assemblages than did wetland type. Although this general relationship was anticipated, the strength of this trend was greater than expected. There were more significant population differences as a function of sheet flow (9) than wetland type (2), and there was a trend across assemblage metrics of higher diversity in flow. The strongest evidence for the importance of flow, relative to wetland type, in structuring assemblages was the low similarity (0.34) between assemblages with and without slow sheet flow, in contrast to the much higher terrestrial and aquatic assemblage similarities as a function of wetland type (0.63 and 0.66, respectively). Insects are sensitive to flow in part because flow lowers water temperature and increases oxygen availability (Erman, 1973; Schowalter, 2006). The high variance and relative lack of trend as a function of wetland type may also be due to the likely multiplicity of faunal sources. For instance, ephemeral waters primarily support lentic and lotic taxa that can tolerate the fluctuating water levels, < ?show=[to]?>but also some animals that are specialized for these habitats, and even some upland and semi-terrestrial taxa (Wiggins et al., 1980; Zedler, 2003). Similarly, upland specialists can be found in terrestrial wetland vegetation (Haslett, 1997; Wettstein and Schmid, 1999). Peatland specific flies make up only about 20% of certain Canadian bog and fen faunas (Marshall, 1994), yet this low percentage is viewed as representing comparatively high peatland specificity, as such percentages are typically lower still (Keiper et al., 2002; Savage et al., 2011). Although classification of wetlands into various types (overview in Mitsch and Gosselink, 2007) has been an important component in both the understanding of larger scale vegetation patterns and in developing wetland conservation measures, these classifications should be extended to faunal assemblages with caution, particularly for aquatic fauna (see also Euliss et al., 2004).

The importance of invertebrates in ecosystem function is widely acknowledged, but invertebrates are often “consigned to the ‘too hard’ basket” (Andersen and Majer, 2004) during design of monitoring programs (see also Agosti et al., 2000; Samways et al., 2010). The inclusion of invertebrates in the NPS Sierra Nevada Inventory and Monitoring Network's Vital Signs is commendable, and our work and that of others (Oliver and Beattie, 1993, 1996; Andersen and Majer, 2004; Underwood and Fisher, 2006) indicate that invertebrates can be sampled and processed efficiently and on a large scale. Our rapid assessment approaches were combined with vegetation and hydrological monitoring, resulting in further efficiencies; multiple sites, all distant from trailheads, were sampled daily throughout each of our field seasons. Invertebrates make up a large portion of the overall abundance, diversity, and food web structure of ecosystems, and simple protocols can capture much of this complexity quickly and easily. We urge other land managers to strongly consider increased emphasis on invertebrates, including terrestrial fauna, in monitoring and research programs. As noted above, however, invertebrate assemblage structure may or may not align with that of vegetation; differing response to some predictors should be anticipated, and is indeed one reason to include invertebrates in ecosystem assessment.