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Aquat Sci (2017) 79:705–717 DOI 10.1007/s00027-017-0530-7

RESEARCH ARTICLE

Hydrology drives seasonal variation in dryland stream macroinvertebrate communities

Xingli Giam1,6  · William Chen2 · Tiffany A. Schriever3 · Richard Van Driesche4 · Rachata Muneepeerakul5 · David A. Lytle4 · Julian D. Olden1 

Received: 13 September 2016 / Accepted: 25 March 2017 / Published online: 3 April 2017 © Springer International Publishing 2017

in intermittent than perennial streams. Hydrology was the main predictor of trait composition; intermittent streams supported a larger fraction of small taxa, taxa with the abil-ity to undergo diapause, and uni- or multivoltine taxa (i.e., taxa with shorter life cycles). Trait composition did not vary across seasons among perennial reaches whereas the fraction of aerial dispersers appeared to be greater in spring than other seasons among intermittent reaches. Our results were largely consistent with predictions of the habitat tem-plet; r-selected traits were more frequently represented in intermittent communities. The temporal characterization of macroinvertebrate community structure in dryland streams provides a powerful glimpse of how stream communities may respond to a drying climate.

Keywords Intermittent flow · Traits-based ecology · Community assembly · Habitat templet · Life history · Ecological filtering

Introduction

The environment is considered paramount in structuring stream communities (Scarsbrook and Townsend 1993; Wil-liams 1996; Poff 1997; Giam and Olden 2016). Among the most environmentally variable systems are stream net-works in dryland regions (rainfall 25–500  mm  year−1), which comprise spatial mosaics of perennial and intermit-tent reaches each with very different temporal hydrologi-cal regimes (Lake 2011; Jaeger and Olden 2012). Given that climate change and increased human water usage are expected to increase drought conditions and stream inter-mittency in many drylands globally (Larned et  al. 2010; Döll and Schmeid 2012; Seager et  al. 2013), elucidating how biotic communities respond to seasonal flow changes

Abstract Many lotic ecosystems are spatially and tempo-rally heterogeneous but none more so than dryland streams flowing through arid and semi-arid landscapes. Under-standing seasonal variation in richness and trait composi-tion is critical to our fundamental understanding of these dynamic stream networks. Here, we analyzed aquatic mac-roinvertebrate communities within perennial and intermit-tent reaches in replicate dryland watersheds in southwest-ern USA across 10 seasons and 4 years. We quantified how hydrology, season, and microhabitat type affected taxa richness and trait composition. Taxa richness was higher in perennial than intermittent reaches, in pools than rif-fles, and in fall and summer than in spring. The interaction between hydrology and season was important; the differ-ence between fall high and spring low richness was greater

Aquatic Sciences

Electronic supplementary material The online version of this article (doi:10.1007/s00027-017-0530-7) contains supplementary material, which is available to authorized users.

* Xingli Giam giamxingli@gmail.com

1 School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA 98105, USA

2 Quantitative Ecology and Resource Management, University of Washington, Seattle, WA 98105, USA

3 Biological Sciences Department, Western Michigan University, Kalamazoo, MI 49008, USA

4 Department of Integrative Biology, Oregon State University, Corvallis, OR 97331, USA

5 Department of Agricultural and Biological Engineering, University of Florida, Gainesville, FL 32611, USA

6 Present Address: Department of Ecology and Evolutionary Biology, The University of Tennessee, Knoxville, TN 37996, USA

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in both perennial and intermittent streams can help inform their likely responses to these future challenges.

Perennial and intermittent streams represent vastly dif-ferent habitats for aquatic macroinvertebrates. In contrast to perennial streams that flow continuously throughout the year, intermittent streams cease flowing periodically resulting in repeated dry-wet cycles (Larned  et al. 2010). The resumption of rainfall-driven surface flow during the wet season drives colonization and establishment of aquatic macroinvertebrates in the previously dry channel. As the wet season transitions into the dry season, reduction of sur-face flow decreases the size, variety, and alters the phys-icochemical characteristics of available habitat patches (Acuña et al. 2005; Bonada et al. 2007; Rolls et al. 2012; Leigh 2013). Eventually, surface flow stops, resulting in a totally dry channel. The lack of surface flow may persist for days to months before arrival of the next wet season and the cycle continues. In dryland systems, supra-annual droughts often punctuate dry-wet cycles (Bogan and Lytle 2011), resulting in an even harsher environment for aquatic macroinvertebrates.

Flow often shapes taxa richness and composition dif-ferences between perennial and intermittent streams. Taxa richness is generally higher in perennial streams than inter-mittent ones (del Rosario and Resh 2000; Bonada et  al. 2006; Fenoglio et al. 2007; García-Roger et al. 2011; Datry 2012; Bogan et al. 2013; Schriever et al. 2015; but see Bon-ada et al. 2007); this is likely driven by greater habitat area, spatial habitat heterogeneity, connectivity, and/or tempo-ral stability in perennial streams (Death and Winterbourne 1995; Ward et al. 1999; Bonada et al. 2007; Datry 2012). Community composition is also often different between intermittent and perennial streams (Bonada et  al. 2006; Datry 2012). In some cases, intermittent communities are nested within perennial communities (Datry 2012), but in other cases they may harbor a specialized fauna of dessica-tion-resistant taxa (Bogan et al. 2013).

Temporal changes in invertebrate communities can result from seasonal dry-wet cycles and associated phys-icochemical changes. In the dry season, habitat area and types are often reduced (from riffles and pools to dry-ing pools), resulting in lower taxa richness or diversity in some systems (Fritz and Dodds 2004; Bêche et  al. 2006; Garcia-Roger  et al. 2011). In other systems, mechanisms are less straightforward and more complicated. In streams in northeastern Spain as well as the Arizona USA streams examined in this study, the increased dominance of lentic pools during the dry season did not result in a reduction in taxa richness because, while lotic Ephemeroptera, Plecop-tera, and Trichoptera (EPT) decreased seasonally, lentic Odonata, Coleoptera, and Hemiptera (OCH) taxa increased in richness (Bogan and Lytle 2007; Bonada et  al. 2007). In northern Australia, lotic taxa are similarly replaced by

lentic taxa that are adapted to the increasingly oxygen-poor and warm water as the dry season proceeds (Leigh 2013).

As the effect of drying is more extreme in intermittent streams, we might expect communities in these streams to be more seasonally variable than perennial communities. While some studies have found this to be true (Bêche et al. 2006; Garcia-Roger et al. 2011 ), others (e.g., Datry 2012) including a recent meta-analysis by Leigh et al. (2016) have not found a consistent effect. A possible reason is that sites investigated by Datry (2012) and Leigh et al. (2016) were sampled before drying began and after the resumption of flow following the dry season, hence the effect of drying might be quickly reversed either by aerial dispersal or mass effects (Urban et  al. 2008; aquatic dispersal of taxa from connected species-rich perennial upstream reaches) (Bogan et al. 2015; Leigh et al. 2016). Alternatively, the temporal stability of intermittent communities may result from the dominance of dessication-resistant taxa (Leigh et al. 2016). Sampling intermittent and perennial sites in one additional time period—at the middle or toward the end of the dry season—might help resolve this question.

Examining traits in addition to taxonomic characteris-tics of communities can yield a more complete understand-ing of flow-ecology relationships as traits are the means by which species interact with and adapt to the environ-ment (Townsend and Hildrew 1994; Lytle and Poff 2004; Mims and Olden 2012). To survive dessication during the dry season, taxa may have traits that enable dispersal from channels as they dry and traits that aid recolonization with flow resumption. These traits, known as resilience traits, include semi-annual or annual life cycles resulting in adult emergence just before channel drying, and the ability to disperse aerially, which allows dispersal between discon-nected waterbodies in the dry season and recolonization of intermittent reaches as flows resume (Stanley et  al. 1994; Bogan et  al. 2015). Traits that enable survival within the dry stream channel (resistance traits) may also contribute to long-term persistence in intermittent streams. Examples of such traits include the ability to undergo diapause (a period in which growth is suspended and metabolic activity is greatly diminished) and the ability to use refuges in the dry channel (Hynes 1970; Robson et al. 2011).

Stream networks in southwestern USA represent a pow-erful and relevant system to study biotic responses to flow variation in drylands. The highly seasonal rainfall drives a complex hydrologic network comprising both perennial and intermittent stream reaches embedded within single watersheds (Sponseller and Fisher 2006; Jaeger and Olden 2012), allowing us to account for inter-watershed variabil-ity in biotic responses. Understanding biotic effects of flow is crucial in this region, which is expected to get drier with climate change (Seager et al. 2013). Previous research has shown that taxonomic composition responds to temporal

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changes in flow in both intermittent (Stanley et  al. 1994) and perennial streams (Bogan and Lytle 2007). It is also clear that taxonomic and feeding group composition dif-fer between intermittent and perennial streams (Bogan and Lytle 2011; Bogan et  al. 2013). More recently, Schriever et al. (2015) demonstrated that functional trait composition differs fundamentally between perennial and intermittent communities, hinting at the importance of trait-environ-ment relationships in structuring taxonomic composition. However, hypotheses regarding affinities of specific traits to different hydrologies, seasons, and microhabitats have yet to be rigorously examined, which limits our understand-ing of how different traits interact with the environment to govern community assembly. Further, mechanisms driving seasonal changes in taxonomic richness in perennial and intermittent streams across multiple years remain unclear.

Here, we examined temporal variation in aquatic macroin-vertebrate communities of perennial and intermittent dryland streams across multiple watersheds in the Upper San Pedro River Basin in Arizona, USA. We quantified how each of three variables—hydrology, season, and microhabitat type (while controlling for the effects of the other two)—drives patterns in taxa richness and trait composition across ten sea-sons over 4 years. We predicted that (1) taxa richness would be higher in perennial reaches, (2) taxa richness would vary seasonally (higher in spring and fall when precipitation run-off is expected to be high) with greater variability in inter-mittent than perennial streams, and (3) trait composition would differ between perennial and intermittent communi-ties and across seasons in accordance with our understand-ing of trait-environment relationships (Table 1). Understand-ing temporal dynamics of community structure in dryland streams would improve our understanding of likely climate change and water use impacts on these communities.

Methods

Study site and sampling methods

Our study focused on intermittent and perennial streams draining the Huachuca Mountains in the Upper San Pedro River Basin of southeastern Arizona, USA. This region experiences highly seasonal rainfall that produces dynamic patterns of stream isolation and connectivity. High-inten-sity, local convective thunderstorms associated with the North American monsoon season, which typically occurs from July to September, bring half of the region’s yearly rainfall. The other half of the yearly precipitation falls from November to April in the form of prolonged, lower magnitude precipitation resulting from Pacific frontal storms. Flow regimes of the study streams are hetero-geneous in both space and time. In general, cascade and

bedrock reaches in the upper canyons draining the moun-tains are perennial whereas step-pool, plane bed and pool-riffle channel forms exhibit more intermittent flows mov-ing downstream. Intermittent reaches flow during the wet winter-fall season and during/after late-summer monsoon storms; they tend to dry up in late spring-early summer between the two wet seasons (Jaeger and Olden 2012).

We sampled aquatic macroinvertebrates at multiple sites along eight perennial reaches and six intermittent reaches from three independent watersheds (Fig.  1). Hydrologic classifications were based on flow data collected by an array of electrical resistance sensors (Jaeger and Olden 2012). Sampling reaches (sites) were surveyed in early fall (FALL), late winter-early spring (SPRING), and early sum-mer (SUMMER) for 4  years; the survey campaign lasted from fall 2009 to fall 2012 (ten seasons in total). However, not all sites were sampled every season owing to person-nel issues and the lack of flow in particular intermittent streams. Whereas perennial reaches flowed on all sampling occasions, intermittent reaches were not flowing for the majority of sampling occasions (see Table  S1, Electronic Supplementary Material for details on flow conditions across sampling occasions for sites).

Within each 100-m long site, we sampled all available pool and riffle microhabitats. The number of pools (0–4) and riffles (0–3) in each site varied among seasons. In riffle microhabi-tats, we scrubbed rocks and agitated stream bed substrates within a 1 m2 area from which dislodged macroinvertebrates were collected in a dip-net downstream. A pool sample con-sisted of a time × area standardized collection of the pool area (benthic, pelagic, and surface) using a 250 μm D-net, with an effort of 10 s per m2 of pool (up to 6 m2 maximum). Macroin-vertebrates were preserved in 95% ethanol and identified to the lowest taxonomic level possible (typically genus/species for insects; family/order for non-insects) in the laboratory. As Chironomidae and Simuliidae were only identified to family level and likely comprised a large number of genera/species, we excluded them from our analyses.

Taxa life‑history traits

We collated data for 4 life-history traits that are linked to colonization ability and population persistence of aquatic macroinvertebrates (Poff et al. 2006). Information from the primary literature, databases, and available expert knowl-edge were used to populate the trait dataset according to Schriever et  al. (2015). The life-history traits were: (1) maximum larval body size (SIZE), (2) ability to undergo diapause (DIAP), (3) voltinism (VOLT), and (4) dispersal strategy (DISP). We present a detailed description of these traits and our hypotheses regarding the variation in trait composition in perennial versus intermittent streams, in dif-ferent microhabitats, and across seasons in Table 1.

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Statistical analyses

Taxa richness patterns

We used generalized linear mixed effects models (GLMMs) to quantify how season, microhabitat type (pool versus rif-fle), and hydrology (perennial versus intermittent) relate

to taxa richness at two spatial scales. First we considered richness at the level of individual microhabitats (“individ-ual microhabitat scale”; n = 183); second, we pooled rich-ness in replicated microhabitats within each reach (“reach scale”; n = 142). For both analyses, taxa richness was mod-elled as a Poisson-distributed quantity (Zuur et  al. 2009). To control for the spatial dependency of microhabitats

Table 1 Description of the 4 traits hypothesized to drive community composition across perennial versus intermittent reaches, microhabitats, and seasons

Our predictions are developed from ecological theory and findings from the literature, which include (in parentheses)a Southwood (1988)b Townsend and Hildrew (1994)c Williams (1996)d Townsend et al. (1997)e Beche et al. (2006)f Bonada et al. (2007)g Townsend and Thompson (2007)h Bogan and Lytle (2011)i Bogan and Lytle (2007)j Thorp and Rogers (2011)k Dell et al. (2014)l Twardochleb and Olden (2016)m Bogan and Boersma (2012)

Traits Trait modalities (categories) Predictions

SIZE: body size Small (<9 mm); medium (9–16 mm); large (>16 mm) Perennial reaches harbor larger taxa; year-round flow allows development of larger body size whereas small body size facilitates survival in hyporheos when inter-mittent stream driesa–h

Riffles contain larger taxa; the coarser substrate in riffles form larger interstitial spaces, which can accommodate larger taxa than the smaller interstitial spaces in poolsg

Smaller taxa preponderant during fall after monsoon and/or in dry season; smaller taxa related to shorter devel-opment times conferring resilience to monsoonal flash floods and/or droughtsb, d, e

DIAP: ability to diapause Yes (diapause or presence of structures for diapause in taxon or close relatives); No (no diapause or absence of structures for diapause in taxon or close relatives)

Taxa with diapause relatively more common in intermit-tent reaches; allows for survival when stream is drya, c,

f, i, j

Relative proportion of taxa with diapause higher in drier seasons; diapause allows for recolonization when flow resumesc, i, j, k

VOLT: voltinism Semivoltine (<1 gen/year); univoltine (1 gen/year); mul-tivoltine (>1 gen/year)

Perennial reaches support more taxa with longer life-cycles; year-round availability of habitata, c, f

Riffles contain more taxa with longer life-cycles; larger and complex substrate increases predator avoidanceg, l

DISP: dispersal strategy Aerial; obligate aquatic Intermittent reaches support relatively more aerial dis-persers; high flow variability and discontinuous habitats disadvantage obligate aquatic dispersersa, c, f

Greater proportion of aerial dispersers in spring and/or summer in intermittent streams; rainfall during winter-spring and summer might trigger aerial dispersers to colonize new habitatsc, m

Greater proportion of aerial dispersers in spring as declining winter-spring flow reduces colonization by obligate aquatic dispersers

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nested within sites and sites nested within independent streams (i.e. watersheds), sites and independent streams were included as random intercepts. We included year as a random intercept to account for possible interannual vari-ation. An observation-level random intercept was fitted to incorporate the extra-Poisson variation (overdispersion) in the observed data (Sekar et al. 2016).

We analyzed the GLMMs in a multimodel inference framework. Candidate GLMMs comprising all possible combinations of fixed effect predictors, and their bivariate interactions were ranked by small-sample Akaike Infor-mation Criteria (AICc) to quantify their relative support (Burnham and Anderson 2002). We selected top-ranked models with ΔAICc values of <2 for inference (Burnham and Anderson 2002). To infer how fixed effect predictors influenced taxa richness, predictions from selected models were averaged using rescaled Akaike model weights (w; the probability that a given top-ranked model is the best). To quantify model goodness-of-fit, we calculated variance explained by fixed effects (marginal R2; R2

m, Nakagawa and Schielzeth 2012).

Functional trait patterns

We examined trait composition of macroinvertebrate com-munities using two complementary approaches. Both anal-yses were conducted at the reach scale to minimize non-independence of replicates of the same microhabitat nested within each reach. First, we used non-metric multidimen-sional scaling (NMDS) to ordinate aggregated microhabitat samples in trait-space based on Bray-Curtis distance; the input matrix was a sample-by-trait matrix that quantifies the number of taxa having each trait modality within each sample. We graphically inspected the resulting ordination plot to infer patterns in trait composition variation among reaches according to hydrological classes, seasons, and microhabitats.

In the second method, we fitted linear mixed models (LMMs) to examine relationships between hydrology, season, and microhabitat and the proportion of taxa pos-sessing each individual trait modality. The response vari-able, despite being a proportion, was modelled as having Gaussian errors because of its simple interpretation and

Fig. 1 Location of study sites (points) and watersheds (grey polygons) in the Huachuca mountains in southeastern Arizona, USA. Inset State of Arizona (shaded grey) and study region (black bounding box)

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satisfactory fit to the data. Using binomial (logit) GLMMs gave similar results; we were therefore confident that our results would be robust to different distributional assump-tions and we present only the Gaussian LMMs for ease of interpretation. As with the taxon richness analysis, site, stream, and years were fitted as random intercepts to incor-porate the spatial and temporal structure of the data. LMMs were analyzed in a multimodel inference framework and models with ΔAICc values <2 were considered plausible and used to infer relationships (Burnham and Anderson 2002). We investigated the effect of microhabitat and sea-son on perennial communities (n = 128), and the effect of hydrology, microhabitat, and season on intermittent and perennial communities. For the latter analysis, we restricted the analysis to seasons where both intermittent and peren-nial communities were successfully sampled (n = 71).

The two approaches are complementary because whereas NMDS detects patterns in multivariate trait com-position, LMMs identifies individual traits that are most strongly related to hydrological, seasonal, and microhabitat differences while controlling for spatial and temporal non-independence among samples. We performed all analy-ses in R v. 3.3.0 (R Core Team 2016). We used the lme4 package (Bates et al. 2016) to fit GLMMs and LMMs, and the vegan package (Oksanen et  al. 2016) for multivariate analyses.

Results

At both individual microhabitat and reach scales, the main effects of hydrology, microhabitat, and season, as well as hydrology-microhabitat and hydrology-season interactions

explained patterns in taxa richness (Fig. 2; Table 2; Fig. S1, Electronic Supplementary Material). The same two models were selected (ΔAICc <2) for both analyses; these fixed effect predictors explained 74% of the variance in indi-vidual microhabitat-scale richness [summed Akaike weight (w) = 0.87], and 42% of the variance in reach-scale richness (w = 0.84).

Taxa richness was higher in perennial reaches than inter-mittent reaches; this was true regardless of microhabitat (Fig. 2; Fig. S1). In both perennial and intermittent reaches, pools had higher taxa richness than riffles, and richness was highest in fall and lowest in spring. A hydrology-sea-son interaction was also clearly observed; seasonal varia-tion in taxa richness at both microhabitat and reach scales was much greater in intermittent streams than in perennial streams. There was also an interaction between hydrology and microhabitat; although pools were always more taxon-rich than riffles, the pool-riffle taxa ratio was greater in intermittent streams.

We found marked differences between trait compositions of intermittent versus perennial reaches in ordination space (2-D, stress = 0.12; Fig.  3). Within each stream network, samples within intermittent reaches tended to comprise a higher proportion of small-sized taxa, taxa with the ability to undergo diapause, and taxa that are uni- or multi-voltine compared to perennial samples (Fig. 3), with the exception of a single pool community in the Garden stream network (Fig. 3b). Communities in pools (Fig. 3b, d, f) versus riffles (Fig.  3c, e, g) appeared to be slightly different. Perennial riffle communities lie to the right of perennial pool com-munities on axis 1, indicating that the former harbored a larger fraction of semivoltine and/or large taxa. Trait com-position did not appear to vary consistently across seasons

Fig. 2 Model-averaged predictions of taxa richness at the individual microhabitat scale across seasons, micro-habitat, and hydrology classes. Transparent symbols represent observed data. Spr spring, Sum summer. See Fig. S1 for model predictions of reach (pooled microhabitats) scale taxa rich-ness

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in perennial reaches. Among intermittent reaches, however, communities during spring appeared to have the highest value on NMDS axis 2, followed by summer, and then fall.

In perennial communities, the proportion of all trait modalities did not differ across seasons nor between micro-habitats, with the exception of semivoltinism (Fig. 4). The null model, which had no fixed effects predictor, was the top model in predicting the relative frequencies of all trait modalities except semivoltinism; the Akaike weight (w) indicated high confidence this was true (w = 0.93–0.99) (Table  3). Semivoltinism was the only trait modality that could be predicted by microhabitat. Riffle samples had a higher proportion of semivoltine taxa compared to pool samples but this effect was modest (Rm

2 = 0.10).Analyzing both perennial and intermittent communi-

ties in tandem revealed that hydrology was most important in driving variation in the proportion of trait modalities. Hydrology was the only predictor present in top models (Table  4). Intermittent communities supported dispropor-tionately more small-sized taxa (w = 0.97; Rm

2 = 0.43) but fewer medium (w = 0.98; Rm

2 = 0.34) and large-sized taxa (w = 0.85; Rm

2 = 0.18) (Fig. 5). Taxa in intermittent streams were also more likely to possess the ability to undergo dia-pause (w = 0.94; Rm

2 = 0.34), and were less likely semi-voltine (w = 0.57; Rm

2 = 0 .16). Dispersal strategy, univol-tinism, and multivoltinism did not appear to be associated with hydrology, season, or microhabitat; the null model was chosen to be the top model for these trait modalities.

Discussion

How communities assemble over time and across space remains a fundamental question in aquatic ecology. This question is especially relevant to dryland streams, which are characterized by heterogeneous flow regimes that lead to considerable spatiotemporal variability in habitat avail-ability and condition. Over the 4-year duration of our study,

perennial reaches of all three streams flowed in all seasons, whereas intermittent reaches ceased to flow during many sampling seasons (Table S1). We expected continuous flow in intermittent streams in early spring (end March–early April), which is near the end of the traditionally high-flow winter season (Bogan et  al. 2013). However, flow was observed in spring 2010 but absent in the spring of 2011 and 2012. This suggests significant inter-annual variability in stream flow; a pattern supported by Jaeger and Olden (2012). Large variation in seasonal flow intermittency across the landscape had profound impacts on community assembly as demonstrated in seasonal patterns of taxa rich-ness and trait composition.

Macroinvertebrate taxa richness varied as a function of hydrology, season, and microhabitat. Our first prediction regarding the effect of hydrology on taxa richness was sup-ported. As expected, at both individual microhabitat and reach scales, perennial communities supported more taxa than intermittent communities did in all seasons. Factors that could have contributed to higher richness in perennial reaches include increased habitat connectivity which pro-motes transportation of resources and taxa dispersal (Ward et  al. 1999), habitat stability (Death and Winterbourne 1995), increased size and diversity of habitats (Bonada et al. 2007), and a greater input of allochthonous resources (Vannote et al. 1980).

Our second prediction was supported in part; taxa richness exhibited greater seasonal variability in intermit-tent streams (Fig.  2). With continuous year-round flow, perennial streams provide temporally stable habitats, thus maintaining relatively consistent taxa richness across seasons in comparison to intermittent streams. However, contrary to our expectation, taxa richness peaked in fall and was lowest in spring in both perennial and intermit-tent reaches. We predicted richness to be relatively high in early spring owing to increased baseflow immediately after the traditionally wet winter season (Bogan et  al. 2013). Flow sensors deployed in intermittent streams

Table 2 Coefficients of top-ranked (ΔAICc <2) generalized linear mixed models (GLMMs) that predict taxa richness as a function of hydrology (H), microhabitat type (M), season (S), their pairwise interactions

w Akaike weight, i.e., the probability of the model being the best among candidate models; R2m proportional variance explained by fixed effects;

Hint intermittent hydrology; Mrf riffle microhabitat; Ssp spring season; Ssu summer season

Model w R2m Coefficients

Hint Mrf Ssp Ssu Hint ×Mrf Hint × Ssp Hint × Ssu Mrf × Ssp Mrf × Ssu

Individual microhabitat-scale richness ~H + M + S + H × M + H × S 0.49 0.74 −0.26 −0.23 −0.15 −0.09 −0.34 −1.22 −0.24 ~H + M + S + H × S 0.38 0.74 −0.52 −0.25 −0.15 −0.08 −1.31 −0.21

Reach-scale richness ~H + M + S + H × S 0.58 0.42 −0.36 −0.27 −0.22 −0.19 −0.90 −0.16 ~H + M + S + H × M + H × S 0.26 0.42 −0.21 −0.26 −0.22 −0.19 −0.21 −0.83 −0.16

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Fig. 3 Non-metric multidimen-sional scaling (NMDS) plots of the positions of a individual trait modalities and b–g reach-scale riffle and pool samples in different streams across differ-ent seasons. Trait modalities are Sm (small size), Md (medium size), Lg (large size), Dp (abil-ity to diapause), NDp (no dia-pause), Ar (aerial disperser), Aq (obligate aquatic disperser), SV (semivoltine), UV (univoltine), and MV (multivoltine). The NMDS solution has a stress of 0.12, indicating a fair fit to the original multivariate data. In e, the sample annotated by (*) has an NMDS 1 value of −1.10

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from 2009 to 2011 found that flow remained intermit-tent in winter (Schriever et  al. 2015), which might help account for our results. Frequent stream drying events in intermittent stream reaches during winter likely acted as a strong habitat filter by removing taxa that could not sur-vive for extended periods on dry stream beds, thus reduc-ing taxa richness. Adult emergence (Velasco and Millan 1998) or aerial dispersal (Bogan et al. 2015) in anticipa-tion of the dry season (between late April and the mon-soon season starting in July) might have also contributed to lower taxa richness in intermittent reaches in spring. Conversely, summer monsoon floods likely enhanced connectivity between the perennial upstream and inter-mittent downstream reaches, thus allowing for increased taxa dispersal and colonization. Further, Bogan and Boersma (2012) found that monsoon storms are a cue for aerial dispersal of some invertebrates. The higher rich-ness in fall relative to summer might also be reflective of the amount of time available for dispersal and coloniza-tion since the stream rewetted from monsoon runoff.

Microhabitat type played an important role in shaping diversity patterns. Pools supported higher taxa richness than riffles in our dryland stream system. By contrast, pre-vious studies in other (non-dryland) stream systems did not find a consistent effect of microhabitat on richness (e.g., Logan and Brooker 1983; Boulton and Lake 1992; Carter and Fend 2001; Bonada et  al. 2006). The higher stabil-ity of pools might have contributed to higher taxa rich-ness (Boulton and Lake 1992). However, the difference in

Fig. 4 Mean proportion of trait modalities in reach-scale commu-nities in perennial a pools and b riffles across seasons. Error bars reflect standard errors. Data include all sampling occasions

Table 3 Coefficients of top-ranked (ΔAICc <2) linear mixed mod-els (LMMs) that relate proportional trait richness within perennial reaches to season (S), microhabitat (M), and their interaction

w Akaike weight, i.e., the probability of the model being the best among candidate models; R2

m variance explained by fixed effects; Mrf coefficient value for riffle microhabitatHydrology, season, and interaction terms were not included in the top-ranked models

Traits Model w R2m Mrf

Body size Small ~1 0.99 0 Medium ~1 0.98 0 Large ~1 0.99 0

Ability to diapause Yes ~1 0.98 0

Dispersal strategy Aerial ~1 0.97 0

Voltinism Semivoltine ~M 0.99 0.10 0.03 Univoltine ~1 0.93 0 Multivoltine ~1 0.93 0

Table 4 Coefficients of top-ranked linear mixed models (LMMs) that relates proportional trait richness among perennial and intermit-tent streams to hydrology (H), microhabitat (M), season (S), and their interactions

w Akaike weight, i.e., the probability of the model being the best among candidate models; R2

m proportional variance explained by fixed effects; Hint coefficient value for intermittent hydrologyMicrohabitat, season, and interaction terms were not included in the top-ranked models

Traits Model w R2m Hint

Body size Small ~H 0.97 0.43 0.18 Medium ~H 0.98 0.34 −0.11 Large ~H 0.85 0.18 −0.07

Ability to diapause Yes ~H 0.94 0.34 0.23

Dispersal strategy Aerial ~1 0.87 0 Voltinism Semivoltine ~H 0.57 0.16 −0.06 Univoltine ~1 0.95 0 Multivoltine ~1 0.88 0

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taxa richness might also reflect the difference in sampling techniques between the microhabitats that was necessary to obtain representative samples. Despite potential issues in comparability of richness between microhabitats, the effects of hydrology and season (as presented above) are robust because models controlled for microhabitat type.

We observed clear differences in functional (trait) com-position between communities in intermittent versus per-ennial reaches, a finding that was consistent with our third prediction. Intermittent reaches were characterized by hav-ing a greater fraction of taxa with small body size, ability to undergo diapause, and uni- and multivoltinism. These traits impart resilience and/or resistance to temporally vary-ing stream conditions in line with predictions of the habitat templet (Townsend and Hildrew 1994; Schriever and Lytle 2016). Taxa with small size and multivoltine life-cycles are classic r-strategists (MacArthur and Wilson 1967) whose rapid growth rates, short life spans, and relatively high fecundity allow timely reproduction before stream dry-ing and quick colonization once intermittent stream flow resumes. Similarly, the ability to survive dry conditions in one or more life-stages allows taxa to persist in  situ in

dry seasons and drought years (Bogan et al. 2013), allow-ing for rapid colonization of existing habitat or dispersal to other intermittent reaches upon flow resumption. Riffles in perennial reaches appeared to be modestly associated with semivoltine taxa; inspection of community data indicated that riffle beetle (Heterelmis sp.—Family Elmidae) and a caddisfly taxon (Wormaldia sp.—Family Philopotamidae), which are semivoltine, were common in riffles and thus contributed to this relationship. Whereas trait composition did not appear to vary in a consistent manner between sea-sons among perennial streams, intermittent communities in spring appeared to support a higher fraction of aerial dispersers than in other seasons (Fig.  5). This result is in partial agreement with our predictions regarding dispersal strategy (Table 1). Aerial dispersers were more numerous in spring and only among intermittent streams because high flow intermittency in winter-early spring likely impeded aquatic dispersal. By contrast, year-round habitat availabil-ity in perennial reaches would not have selectively favored taxa with traits that confer an advantage in highly variable environments.

Fig. 5 Mean proportion of trait modalities in reach-scale commu-nities in a perennial pools, b intermittent pools, c perennial riffles, and d intermittent riffles across seasons. Error bars reflect standard

errors. Data include only sampling occasions in which both perennial and intermittent habitats were available

715Hydrology drives seasonal variation in dryland stream macroinvertebrate communities

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By modelling patterns in trait modality we strengthened the inferences drawn from the multivariate analysis. Across all stream reaches, hydrology was the most important vari-able in predicting the proportion of macroinvertebrate com-munities characterized by taxa in various size categories, ability to diapause, and voltinism. This suggests consider-able species sorting based on functional trait adaptations to flow intermittency, and that mass effects exerted relatively little influence on species communities. If mass effects were more important, we would expect passive dispersal to dilute differences in trait composition between perennial and intermittent sites once flow resumes in the latter habi-tat. Moreover, we did not detect a hydrology-season inter-action, which would be expected if trait composition in per-ennial and intermittent communities homogenized in the summer monsoon season (when intermittent reaches first reconnect to upstream perennial reaches) before diverging in fall as flow stabilized and communities equilibrated.

Among perennial reaches, the proportion of taxa in all trait modalities, with the exception of semivoltinism, were similar across seasons and between habitats, sug-gesting considerable spatiotemporal homogeneity in func-tional composition. Riffles were weakly correlated with an increase in the fraction of semivoltine taxa, supporting our conclusions from the NMDS analysis. We did not formally model seasonal effects among intermittent reaches because we had few replicates across seasons, which reflected the unpredictability of flow in intermittent reaches of dryland stream systems. We were thus unable to confirm the effect of season on dispersal strategy (as inferred from the NMDS ordination) among intermittent streams.

Traits associated with intermittent versus perennial streams in our study were similar to those identified in the Mediterranean-climate streams in northeastern Spain (Bonada et  al. 2007). This indicates some generality in trait-environment relationships across streams in different climates. A formal meta-analysis that uses a single stand-ardized framework to analyze multiple datasets (e.g., Datry et al. 2014; Leigh et al. 2016) could examine whether the strength of these relationships differ across latitudinal or flow permanence gradient. Whereas Bêche et  al. (2006) found clear seasonal variation in trait composition in both perennial and intermittent Mediterranean-climate streams in California, there was little indication that season affected trait composition of perennial reaches in our study. Differ-ences in seasonality in rainfall and thus flow could partially explain the discrepancy; the Mediterranean-climate streams studied by Bêche et al. (2006) had a longer winter wet sea-son (from November to May) and lacked the summer mon-soon observed in our dryland streams. The lower annual rainfall in dryland streams might have also imposed a strict habitat filter at the landscape level, resulting in lower sea-sonal trait variation.

With climate change and increasing human water abstraction, an increasing number of perennial streams in dryland stream systems are projected to become intermit-tent (Larned et  al. 2010) including the ones studied here (Seager et  al. 2013; Jaeger et  al. 2014). Mediterranean stream systems are expected to experience drier condi-tions and an increased number of droughts, thus resem-bling dryland streams (Filipe et al. 2013). By characteriz-ing changes in aquatic macroinvertebrate communities in different microhabitats within perennial and intermittent reaches across seasons in multiple years, our study pro-vides an indication of how these communities in dryland and Mediterranean stream systems may respond to climate change and increased human water use. Taxa richness at both microhabitat and reach scales are expected to decline across all seasons, and seasonal richness differences would likely become more pronounced as more dryland stream reaches transition from perennial to intermittent flow, and as Mediterranean-climate streams experience more dry-land-like conditions. We expect changes in taxa richness to be accompanied by an increase in the proportion of small-bodied taxa, multivoltine taxa, and taxa that possess the ability to undergo diapause. Given the prospect of losing taxonomic and trait diversity, further long-term research is required to not just document these potential changes, but also understand their effects on stream ecosystem function.

Acknowledgements Funding was provided by the US Department of Defense (SERDP RC-1724, RC-2203, RC-2511). We thank Sheri-dan Stone for logistical support at Fort Huachuca, and Brooke Gebow and the Nature Conservancy for access to streams and lodging at the Ramsey Canyon Preserve, Arizona. This manuscript benefited from the valuable comments of two anonymous reviewers.

Author contributions XG led writing of the manuscript. XG and WC analysed data. JDO and DAL designed study. DAL and TAS per-formed field work and collated trait data. RVD led taxonomic identifi-cations. All authors contributed to the writing of the manuscript.

References

Acuña VM, Muñoz I, Giorgi A, Omella M, Sabater F, Sabater S (2005) Drought and postdrought recovery cycles in an intermit-tent Mediterranean stream: structural and functional aspects. J N Am Benthol Soc 24:919–933

Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Sing-mann H, Dai B, Grothendieck G, Green P (2016) lme4: linear mixed-effects models using ‘Eigen’ and S4, 1.1–12. https://cran.r-project.org/web/packages/lme4/index.html. Accessed Sept 2016

Bêche LA, McElravy EP, Resh VH (2006) Long-term seasonal variation in the biological traits of benthic-macroinvertebrates in two Mediterranean-climate streams in California, U.S.A. Freshw Biol 51:56–75

Bogan MT, Boersma KS (2012) Aerial dispersal of aquatic inver-tebrates along and away from arid-land streams. Freshw Sci 31:1131–1144

716 X. Giam et al.

1 3

Bogan MT, Lytle DA (2007) Seasonal flow variation allows ‘time-sharing’ by disparate aquatic insect communities in montane desert streams. Freshw Biol 52:290–304

Bogan MT, Lytle DA (2011) Severe drought drives novel com-munity trajectories in desert stream pools. Freshw Biol 56:2070–2081

Bogan MT, Boersma KS, Lytle DA (2013) Flow intermittency alters longitudinal patterns of invertebrate diversity and assem-blage composition in an arid-land stream network. Freshw Biol 58:1016–1028

Bogan MT, Boersma KS, Lytle DA (2015) Resistance and resil-ience of invertebrate communities to seasonal and suprasea-sonal drought in arid-land headwater streams. Freshw Biol 60:2547–2558

Bonada N, Rieradevall M, Prat N, Resh VH (2006) Benthic mac-roinvertebrate assemblages and macrohabitat connectivity in Mediterranean-climate streams of northern California. J N Am Benthol Soc 25:32–43

Bonada N, Rieradevall M, Prat N (2007) Macroinvertebrate commu-nity structure and biological traits related to flow permanence in a Mediterranean river network. Hydrobiologia 589:91–106

Boulton AJ, Lake PS (1992) The ecology of two intermittent streams in Victoria, Australia. II. Comparisons of faunal composition between habitats, rivers and years. Freshw Biol 27:99–121

Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd  edn. Springer, New York

Carter JL, Fend SV (2001) Inter-annual changes in the benthic com-munity structure of riffles and pools in reaches of contrasting gradient. Hydrobiologia 459:187–200

Datry T (2012) Benthic and hyporheic invertebrate assemblages along a flow intermittence gradient: effects of duration of dry events. Freshw Biol 57:563–574

Datry T, Larned ST, Fritz KM, Bogan MT, Wood PJ, Meyer EI, San-tos AN (2014) Broad-scale patterns of invertebrate richness and community composition in temporary rivers: effects of flow intermittence. Ecography 37:94–104

Death RG, Winterbourne MJ (1995) Diversity patterns in stream ben-thic invertebrate communities: the influence of habitat stability. Ecology 76:1446–1460

del Rosario R, Resh VH (2000) Invertebrates in intermittent and per-ennial streams: is the hyporheic zone a refuge from drying. J N Am Benthol Soc 19:680–696

Dell AI, Alford RA, Pearson RG (2014) Intermittent pool beds are permanent cyclic habitats with distinct wet, moist and dry phases. PLoS One 9:e108203. doi:10.1371/journal.pone.0108203

Döll P, Schmeid HM (2012) How is the impact of climate change on river flow regimes related to the impact on mean annual runoff? A global-scale analysis. Environ Res Lett 7:014037

Fenoglio S, Bo T, Cucco M, Malacarne G (2007) Response of benthic invertebrate assemblages to varying drought conditions in the Po river (NW Italy). Italian J Zool 74:191–201

Filipe AF, Lawrence JE, Bonada N (2013) Vulnerability of stream biota to climate change in mediterranean climate regions: a syn-thesis of ecological responses and conservation challenges. Hyd-robiologia 719:331–351

Fritz KM, Dodds WK (2004) Resistance and resilience of macroin-vertebrate assemblages to drying and flood in a tallgrass prairie stream system. Hydrobiologia 527:99–112

García-Roger EM, Sánchez-Montoya MdM, Gomez R, Suárez ML, Vidal-Abarca MR, Latron J, Rieradevall M, Prat N (2011) Do seasonal changes in habitat features influence aquatic macroin-vertebrate assemblages in perennial versus temporary Mediter-ranean streams? Aquat Sci 73:567–579

Giam X, Olden JD (2016) Environment and predation govern fish community assembly in temperate streams. Glob Ecol Biogeogr. doi:10.1111/geb.12475

Hynes HBN (1970) The ecology of stream insects. Annu Rev Entol-mol 15:25–42

Jaeger KL, Olden JD (2012) Electrical resistance sensor arrays as a means to quantify longitudinal connectivity of rivers. River Res Appl 28:1843–1852

Jaeger KL, Olden JD, Pelland NA (2014) Climate change poised to threaten hydrologic connectivity and endemic fishes in dryland streams. Proc Natl Acad Sci 111:13894–13899

Lake PS (2011) Drought and aquatic ecosystems: effects and responses, 1st edn. Blackwell, Oxford

Larned ST, Datry T, Arscott DB, Tockner K (2010) Emerging con-cepts in temporary-river ecology. Freshw Biol 55:717–738

Leigh C (2013) Dry-season changes in macroinvertebrate assem-blages of highly seasonal rivers: responses to low flow, no flow and antecedent hydrology. Hydrobiologia 703:95–112

Leigh C, Bonada N, Boulton AJ, Hugueny B, Larned ST, Vander Vor-ste R, Datry T (2016) Invertebrate assemblage responses and the dual roles of resistance and resilience to drying in intermittent rivers. Aquat Sci 78:291–301

Logan P, Brooker MP (1983) The macroinvertebrate faunas of riffles and pools. Water Res 17:263–270

Lytle DA, Poff NL (2004) Adaptation to natural flow regimes. Trends Ecol Evol 19:94–100

MacArthur RH, Wilson EO (1967) The Theory of Island Biogeogra-phy. Princeton University Press, Princeton, NJ

Mims MC, Olden JD (2012) Life history theory predicts fish assem-blage response to hydrologic regimes. Ecology 93:35–45

Nakagawa S, Schielzeth H (2012) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Method Ecol Evol 4:133–142

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) vegan: Community Ecology Package, v. 2.3–5. https://cran.r-project.org/web/packages/vegan/index.html. Accessed Sept 2016

Poff NL (1997) Landscape filters and species traits: towards mecha-nistic understanding and prediction in stream ecology. J N Am Benthol Soc 16:391–409

Poff NL, Olden JD, Vieira NKM, Finn DS, Simmons MP, Kondra-tieff BC (2006) Functional trait niches of North American lotic insects: traits-based ecological applications in light of phyloge-netic relationships. J N Am Benthol Soc 25:730–755

R Core Team (2016) R: a language and environment for statistical computing, v. 3.3.0. R Foundation for Statistical Computing, Vienna. https://www.R-project.org. Accessed Sept 2016

Robson BJ, Chester ET, Austin CM (2011) Why life history informa-tion matters: drought refuges and macroinvertebrate persistence in non-perennial streams subject to a drier climate. Mar Freshw Res 62:801–810

Rolls RJ, Leigh C, Sheldon F (2012) Mechanistic effects of low-flow hydrology on riverine ecosystems: ecological principles and con-sequences of alteration. Freshw Sci 31:1163–1186

Scarsbrook MR, Townsend CR (1993) Stream community structure in relation to spatial and temporal variation: a habitat templet study of two contrasting New Zealand streams. Freshw Biol 29:395–410

Schriever TA, Lytle DA (2016) Convergent diversity and trait compo-sition in temporary streams and ponds. Ecosphere. doi:10.1002/ecs2.1350

Schriever TA., Bogan MT, Boersma KS, Cañedo-Argüelles M, Jaeger KL, Olden JD, Lytle DA (2015) Hydrology shapes taxonomic and functional structure of desert stream invertebrate communi-ties. Freshw Sci 34:399–409

717Hydrology drives seasonal variation in dryland stream macroinvertebrate communities

1 3

Seager R, Ting M, Li C, Naik N, Cook B, Nakamura J, Liu H (2013) Projections of declining surface-water availability for the south-western United States. Nat Clim Change 3:482–486

Sekar N, Giam X, Sharma NP, Sukumar R (2016) How much Dille-nia indica seed predation occurs from Asian elephant dung? Acta Oecologica 70:53–59

Southwood TRE (1988) Tactics, strategies and templets. Oikos 52:3–18

Sponseller RA, Fisher SG (2006) Drainage size, stream intermittency, and ecosystem function in a Sonoran Desert Landscape. Ecosys-tems 9:344–356

Stanley EH, Buschman DL, Boulton AJ, Grimm NB, Fisher SG (1994) Invertebrate resistance and resilience to intermittency in a desert stream. Am Midl Nat 131:288–300

Thorp JH, Rogers DC (2011) Field Guide to Freshwater Invertebrates of North America. Academic Press, San Diego, CA

Townsend CR, Hildrew AG (1994) Species traits in relation to a habi-tat templet for river systems. Freshw Biol 31:265–275

Townsend CR, Thompson RM (2007) Body size in streams: mac-roinvertebrate community size composition along natural and human-induced environmental gradients. In: Hildrew AG, Raf-faelli DG, Edmonds-Brown R (eds) Body size: the structure and function of aquatic ecosystems. Cambridge University Press, Cambridge, pp 77–79

Townsend CR, Dolédec S, Scarsbrook MR (1997) Species traits in relation to temporal and spatial heterogeneity in streams: a test of habitat templet theory. Freshw Biol 27:367–387

Twardochleb LA, Olden JD (2016) Human development modifies the functional composition of lake littoral communities. Hydrobio-logia. doi:10.1007/s10750-016-2727-5

Urban MC, Leibold MA, Amerasekare P, De Meester L, Gomulkie-wicz R, Hochberg ME, Klausmeier CA, Loeuille N, de Mazan-court C, Norberg J, Pantel JH, Strauss SY, Vellend M, Wade MJ (2008) The evolutionary ecology of metacommunities. Trends Ecol Evol 23:311–317

Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137

Velasco J, Millan A (1998) Insect dispersal in a drying desert stream: effects of temperature and water loss. Southwest Nat 43:80–87

Ward JV, Tockner K, Schiemer F (1999) Biodiversity of floodplain river ecosystems: ecotones and connectivity. Regul Rivers: Res Mgmt 15:125–139

Williams DD (1996) Environmental constraints in temporary fresh-waters and their consequences for the insect fauna. J N Am Benthol Soc 15:634–650

Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (eds) (2009) Mixed effects models and extensions in ecology with R. Springer, New York