Hydrology Drives Seasonal Variation in Dryland Stream Macroinvertebrate Communities

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

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

Abstract Many lotic ecosystems are spatially and tempo- in intermittent than perennial streams. Hydrology was the rally heterogeneous but none more so than dryland streams main predictor of trait composition; intermittent streams flowing through arid and semi-arid landscapes. Under- supported a larger fraction of small taxa, taxa with the abil- standing seasonal variation in richness and trait composi- ity to undergo diapause, and uni- or multivoltine taxa (i.e., tion is critical to our fundamental understanding of these taxa with shorter life cycles). Trait composition did not dynamic stream networks. Here, we analyzed aquatic mac- vary across seasons among perennial reaches whereas the roinvertebrate communities within perennial and intermit- fraction of aerial dispersers appeared to be greater in spring tent reaches in replicate dryland watersheds in southwest- than other seasons among intermittent reaches. Our results ern USA across 10 seasons and 4 years. We quantified how were largely consistent with predictions of the habitat tem- hydrology, season, and microhabitat type affected taxa plet; r-selected traits were more frequently represented in richness and trait composition. Taxa richness was higher intermittent communities. The temporal characterization of in perennial than intermittent reaches, in pools than rif- macroinvertebrate community structure in dryland streams fles, and in fall and summer than in spring. The interaction provides a powerful glimpse of how stream communities between hydrology and season was important; the differ- may respond to a drying climate. ence between fall high and spring low richness was greater Keywords Intermittent flow · Traits-based ecology · Community assembly · Habitat templet · Life history · Electronic supplementary material The online version of this Ecological filtering article (doi:10.1007/s00027-017-0530-7) contains supplementary material, which is available to authorized users.

* Xingli Giam Introduction [email protected] The environment is considered paramount in structuring 1 School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA 98105, USA stream communities (Scarsbrook and Townsend 1993; Wil- liams 1996; Poff 1997; Giam and Olden 2016). Among 2 Quantitative Ecology and Resource Management, University of Washington, Seattle, WA 98105, USA the most environmentally variable systems are stream networks in dryland regions (rainfall 25–500 mm year−1), 3 Biological Sciences Department, Western Michigan University, Kalamazoo, MI 49008, USA which comprise spatial mosaics of perennial and intermittent reaches each with very different temporal hydrologi- 4 Department of Integrative Biology, Oregon State University, Corvallis, OR 97331, USA cal regimes (Lake 2011; Jaeger and Olden 2012). Given that climate change and increased human water usage are 5 Department of Agricultural and Biological Engineering, University of Florida, Gainesville, FL 32611, USA expected to increase drought conditions and stream intermittency in many drylands globally (Larned et al. 2010; 6 Present Address: Department of Ecology and Evolutionary Biology, The University of Tennessee, Knoxville, TN 37996, Döll and Schmeid 2012; Seager et al. 2013), elucidating USA how biotic communities respond to seasonal flow changes

Vol.:(0123456789)1 3 706 X. Giam et al. in both perennial and intermittent streams can help inform lentic taxa that are adapted to the increasingly oxygen-poor their likely responses to these future challenges. and warm water as the dry season proceeds (Leigh 2013). Perennial and intermittent streams represent vastly dif- As the effect of drying is more extreme in intermittent ferent habitats for aquatic macroinvertebrates. In contrast streams, we might expect communities in these streams to to perennial streams that flow continuously throughout be more seasonally variable than perennial communities. the year, intermittent streams cease flowing periodically While some studies have found this to be true (Bêche et al. resulting in repeated dry-wet cycles (Larned et al. 2010). 2006; Garcia-Roger et al. 2011 ), others (e.g., Datry 2012) The resumption of rainfall-driven surface flow during the including a recent meta-analysis by Leigh et al. (2016) have wet season drives colonization and establishment of aquatic not found a consistent effect. A possible reason is that sites macroinvertebrates in the previously dry channel. As the investigated by Datry (2012) and Leigh et al. (2016) were wet season transitions into the dry season, reduction of sur- sampled before drying began and after the resumption of face flow decreases the size, variety, and alters the phys- flow following the dry season, hence the effect of drying icochemical characteristics of available habitat patches might be quickly reversed either by aerial dispersal or mass (Acuña et al. 2005; Bonada et al. 2007; Rolls et al. 2012; effects (Urban et al. 2008; aquatic dispersal of taxa from Leigh 2013). Eventually, surface flow stops, resulting in a connected species-rich perennial upstream reaches) (Bogan totally dry channel. The lack of surface flow may persist et al. 2015; Leigh et al. 2016). Alternatively, the temporal for days to months before arrival of the next wet season stability of intermittent communities may result from the and the cycle continues. In dryland systems, supra-annual dominance of dessication-resistant taxa (Leigh et al. 2016). droughts often punctuate dry-wet cycles (Bogan and Lytle Sampling intermittent and perennial sites in one additional 2011), resulting in an even harsher environment for aquatic time period—at the middle or toward the end of the dry macroinvertebrates. season—might help resolve this question. Flow often shapes taxa richness and composition dif- Examining traits in addition to taxonomic characteris- ferences between perennial and intermittent streams. Taxa tics of communities can yield a more complete understand- richness is generally higher in perennial streams than inter- ing of flow-ecology relationships as traits are the means mittent ones (del Rosario and Resh 2000; Bonada et al. by which species interact with and adapt to the environ- 2006; Fenoglio et al. 2007; García-Roger et al. 2011; Datry ment (Townsend and Hildrew 1994; Lytle and Poff 2004; 2012; Bogan et al. 2013; Schriever et al. 2015; but see Bon- Mims and Olden 2012). To survive dessication during the ada et al. 2007); this is likely driven by greater habitat area, dry season, taxa may have traits that enable dispersal from spatial habitat heterogeneity, connectivity, and/or tempo- channels as they dry and traits that aid recolonization with ral stability in perennial streams (Death and Winterbourne flow resumption. These traits, known as resilience traits, 1995; Ward et al. 1999; Bonada et al. 2007; Datry 2012). include semi-annual or annual life cycles resulting in adult Community composition is also often different between emergence just before channel drying, and the ability to intermittent and perennial streams (Bonada et al. 2006; disperse aerially, which allows dispersal between discon- Datry 2012). In some cases, intermittent communities are nected waterbodies in the dry season and recolonization of nested within perennial communities (Datry 2012), but in intermittent reaches as flows resume (Stanley et al. 1994; other cases they may harbor a specialized fauna of dessica- Bogan et al. 2015). Traits that enable survival within the tion-resistant taxa (Bogan et al. 2013). dry stream channel (resistance traits) may also contribute to Temporal changes in invertebrate communities can long-term persistence in intermittent streams. Examples of result from seasonal dry-wet cycles and associated phys- such traits include the ability to undergo diapause (a period icochemical changes. In the dry season, habitat area and in which growth is suspended and metabolic activity is types are often reduced (from riffles and pools to dry- greatly diminished) and the ability to use refuges in the dry ing pools), resulting in lower taxa richness or diversity in channel (Hynes 1970; Robson et al. 2011). some systems (Fritz and Dodds 2004; Bêche et al. 2006; Stream networks in southwestern USA represent a pow- Garcia-Roger et al. 2011). In other systems, mechanisms erful and relevant system to study biotic responses to flow are less straightforward and more complicated. In streams variation in drylands. The highly seasonal rainfall drives in northeastern Spain as well as the Arizona USA streams a complex hydrologic network comprising both perennial examined in this study, the increased dominance of lentic and intermittent stream reaches embedded within single pools during the dry season did not result in a reduction in watersheds (Sponseller and Fisher 2006; Jaeger and Olden taxa richness because, while lotic Ephemeroptera, Plecop- 2012), allowing us to account for inter-watershed variabil- tera, and Trichoptera (EPT) decreased seasonally, lentic ity in biotic responses. Understanding biotic effects of flow Odonata, Coleoptera, and Hemiptera (OCH) taxa increased is crucial in this region, which is expected to get drier with in richness (Bogan and Lytle 2007; Bonada et al. 2007). climate change (Seager et al. 2013). Previous research has In northern Australia, lotic taxa are similarly replaced by shown that taxonomic composition responds to temporal

1 3 707 Hydrology drives seasonal variation in dryland stream macroinvertebrate communities changes in flow in both intermittent (Stanley et al. 1994) bedrock reaches in the upper canyons draining the moun- and perennial streams (Bogan and Lytle 2007). It is also tains are perennial whereas step-pool, plane bed and pool- clear that taxonomic and feeding group composition dif- riffle channel forms exhibit more intermittent flows -mov fer between intermittent and perennial streams (Bogan and ing downstream. Intermittent reaches flow during the wet Lytle 2011; Bogan et al. 2013). More recently, Schriever winter-fall season and during/after late-summer monsoon et al. (2015) demonstrated that functional trait composition storms; they tend to dry up in late spring-early summer differs fundamentally between perennial and intermittent between the two wet seasons (Jaeger and Olden 2012). communities, hinting at the importance of trait-environ- We sampled aquatic macroinvertebrates at multiple sites ment relationships in structuring taxonomic composition. along eight perennial reaches and six intermittent reaches However, hypotheses regarding affinities of specific traits from three independent watersheds (Fig. 1). Hydrologic to different hydrologies, seasons, and microhabitats have classifications were based on flow data collected by an yet to be rigorously examined, which limits our understand- array of electrical resistance sensors (Jaeger and Olden ing of how different traits interact with the environment to 2012). Sampling reaches (sites) were surveyed in early fall govern community assembly. Further, mechanisms driving (FALL), late winter-early spring (SPRING), and early sum- seasonal changes in taxonomic richness in perennial and mer (SUMMER) for 4 years; the survey campaign lasted intermittent streams across multiple years remain unclear. from fall 2009 to fall 2012 (ten seasons in total). However, Here, we examined temporal variation in aquatic macroin- not all sites were sampled every season owing to person- vertebrate communities of perennial and intermittent dryland nel issues and the lack of flow in particular intermittent streams across multiple watersheds in the Upper San Pedro streams. Whereas perennial reaches flowed on all sampling River Basin in Arizona, USA. We quantified how each of occasions, intermittent reaches were not flowing for the three variables—hydrology, season, and microhabitat type majority of sampling occasions (see Table S1, Electronic (while controlling for the effects of the other two)—drives Supplementary Material for details on flow conditions patterns in taxa richness and trait composition across ten sea- across sampling occasions for sites). sons over 4 years. We predicted that (1) taxa richness would Within each 100-m long site, we sampled all available pool be higher in perennial reaches, (2) taxa richness would vary and riffle microhabitats. The number of pools (0–4) and riffles seasonally (higher in spring and fall when precipitation run- (0–3) in each site varied among seasons. In riffle microhabi- off is expected to be high) with greater variability in inter- tats, we scrubbed rocks and agitated stream bed substrates mittent than perennial streams, and (3) trait composition within a 1 m2 area from which dislodged macroinvertebrates would differ between perennial and intermittent communi- were collected in a dip-net downstream. A pool sample con- ties and across seasons in accordance with our understand- sisted of a time × area standardized collection of the pool area ing of trait-environment relationships (Table 1). Understand- (benthic, pelagic, and surface) using a 250 μm D-net, with an ing temporal dynamics of community structure in dryland effort of 10 s per m2 of pool (up to 6 m2 maximum). Macroin- streams would improve our understanding of likely climate vertebrates were preserved in 95% ethanol and identified to change and water use impacts on these communities. 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 Methods level and likely comprised a large number of genera/species, we excluded them from our analyses. Study site and sampling methods Taxa life‑history traits Our study focused on intermittent and perennial streams draining the Huachuca Mountains in the Upper San Pedro We collated data for 4 life-history traits that are linked to River Basin of southeastern Arizona, USA. This region colonization ability and population persistence of aquatic experiences highly seasonal rainfall that produces dynamic macroinvertebrates (Poff et al. 2006). Information from the patterns of stream isolation and connectivity. High-inten- primary literature, databases, and available expert knowl- sity, local convective thunderstorms associated with the edge were used to populate the trait dataset according to North American monsoon season, which typically occurs Schriever et al. (2015). The life-history traits were: (1) from July to September, bring half of the region’s yearly maximum larval body size (SIZE), (2) ability to undergo rainfall. The other half of the yearly precipitation falls diapause (DIAP), (3) voltinism (VOLT), and (4) dispersal from November to April in the form of prolonged, lower strategy (DISP). We present a detailed description of these magnitude precipitation resulting from Pacific frontal traits and our hypotheses regarding the variation in trait storms. Flow regimes of the study streams are hetero- composition in perennial versus intermittent streams, in dif- geneous in both space and time. In general, cascade and ferent microhabitats, and across seasons in Table 1.

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Table 1 Description of the 4 traits hypothesized to drive community composition across perennial versus intermittent reaches, microhabitats, and seasons 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 intermittent stream dries a–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 pools g Smaller taxa preponderant during fall after monsoon and/ or in dry season; smaller taxa related to shorter development 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 Taxa with diapause relatively more common in intermit- taxon or close relatives); No (no diapause or absence of tent reaches; allows for survival when stream is drya, c, structures for diapause in taxon or close relatives) 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- Perennial reaches support more taxa with longer life- tivoltine (>1 gen/year) cycles; year-round availability of habitat a, 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 dispersers; high flow variability and discontinuous habitats disadvantage obligate aquatic dispersers a, 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

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)

Statistical analyses to taxa richness at two spatial scales. First we considered richness at the level of individual microhabitats (“individ- Taxa richness patterns ual microhabitat scale”; n = 183); second, we pooled richness in replicated microhabitats within each reach (“reach We used generalized linear mixed effects models (GLMMs) scale”; n = 142). For both analyses, taxa richness was mod- to quantify how season, microhabitat type (pool versus rif- elled as a Poisson-distributed quantity (Zuur et al. 2009). fle), and hydrology (perennial versus intermittent) relate To control for the spatial dependency of microhabitats

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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) nested within sites and sites nested within independent Functional trait patterns streams (i.e. watersheds), sites and independent streams were included as random intercepts. We included year as a We examined trait composition of macroinvertebrate com- random intercept to account for possible interannual vari- munities using two complementary approaches. Both anal- ation. An observation-level random intercept was fitted to yses were conducted at the reach scale to minimize non- incorporate the extra-Poisson variation (overdispersion) in independence of replicates of the same microhabitat nested the observed data (Sekar et al. 2016). within each reach. First, we used non-metric multidimen- We analyzed the GLMMs in a multimodel inference sional scaling (NMDS) to ordinate aggregated microhabitat framework. Candidate GLMMs comprising all possible samples in trait-space based on Bray-Curtis distance; the combinations of fixed effect predictors, and their bivariate input matrix was a sample-by-trait matrix that quantifies interactions were ranked by small-sample Akaike Infor- the number of taxa having each trait modality within each mation Criteria (AIC c) to quantify their relative support sample. We graphically inspected the resulting ordination (Burnham and Anderson 2002). We selected top-ranked plot to infer patterns in trait composition variation among models with ΔAICc values of <2 for inference (Burnham reaches according to hydrological classes, seasons, and and Anderson 2002). To infer how fixed effect predictors microhabitats. influenced taxa richness, predictions from selected models In the second method, we fitted linear mixed models were averaged using rescaled Akaike model weights (w; (LMMs) to examine relationships between hydrology, the probability that a given top-ranked model is the best). season, and microhabitat and the proportion of taxa pos- To quantify model goodness-of-fit, we calculated variance sessing each individual trait modality. The response vari- 2 2 explained by fixed effects (marginal R ; R m, Nakagawa and able, despite being a proportion, was modelled as having Schielzeth 2012). Gaussian errors because of its simple interpretation and

1 3 710 X. Giam et al. satisfactory fit to the data. Using binomial (logit) GLMMs explained patterns in taxa richness (Fig. 2; Table 2; Fig. S1, gave similar results; we were therefore confident that our Electronic Supplementary Material). The same two models results would be robust to different distributional assump- were selected (ΔAICc <2) for both analyses; these fixed tions and we present only the Gaussian LMMs for ease of effect predictors explained 74% of the variance in indi- interpretation. As with the taxon richness analysis, site, vidual microhabitat-scale richness [summed Akaike weight stream, and years were fitted as random intercepts to incor- (w) = 0.87], and 42% of the variance in reach-scale richness porate the spatial and temporal structure of the data. LMMs (w = 0.84). were analyzed in a multimodel inference framework and Taxa richness was higher in perennial reaches than inter- models with ΔAICc values <2 were considered plausible mittent reaches; this was true regardless of microhabitat and used to infer relationships (Burnham and Anderson (Fig. 2; Fig. S1). In both perennial and intermittent reaches, 2002). We investigated the effect of microhabitat and sea- pools had higher taxa richness than riffles, and richness son on perennial communities (n = 128), and the effect of was highest in fall and lowest in spring. A hydrology-sea- hydrology, microhabitat, and season on intermittent and son interaction was also clearly observed; seasonal varia- perennial communities. For the latter analysis, we restricted tion in taxa richness at both microhabitat and reach scales the analysis to seasons where both intermittent and peren- was much greater in intermittent streams than in perennial nial communities were successfully sampled (n = 71). streams. There was also an interaction between hydrology The two approaches are complementary because and microhabitat; although pools were always more taxon- whereas NMDS detects patterns in multivariate trait com- rich than riffles, the pool-riffle taxa ratio was greater in position, LMMs identifies individual traits that are most intermittent streams. strongly related to hydrological, seasonal, and microhabitat We found marked differences between trait compositions differences while controlling for spatial and temporal non- of intermittent versus perennial reaches in ordination space independence among samples. We performed all analy- (2-D, stress = 0.12; Fig. 3). Within each stream network, ses in R v. 3.3.0 (R Core Team 2016). We used the lme4 samples within intermittent reaches tended to comprise a package (Bates et al. 2016) to fit GLMMs and LMMs, and higher proportion of small-sized taxa, taxa with the ability the vegan package (Oksanen et al. 2016) for multivariate to undergo diapause, and taxa that are uni- or multi-voltine analyses. 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 Results (Fig. 3c, e, g) appeared to be slightly different. Perennial riffle communities lie to the right of perennial pool com- At both individual microhabitat and reach scales, the main munities on axis 1, indicating that the former harbored a effects of hydrology, microhabitat, and season, as well as larger fraction of semivoltine and/or large taxa. Trait com- hydrology-microhabitat and hydrology-season interactions position did not appear to vary consistently across seasons

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

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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

2 Model w R m 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

2 w Akaike weight, i.e., the probability of the model being the best among candidate models; R m proportional variance explained by fixed effects; Hint intermittent hydrology; Mrf riffle microhabitat; Ssp spring season; Ssu summer season in perennial reaches. Among intermittent reaches, however, perennial reaches of all three streams flowed in all seasons, communities during spring appeared to have the highest whereas intermittent reaches ceased to flow during many value on NMDS axis 2, followed by summer, and then fall. sampling seasons (Table S1). We expected continuous flow In perennial communities, the proportion of all trait in intermittent streams in early spring (end March–early modalities did not differ across seasons nor between micro- April), which is near the end of the traditionally high-flow habitats, with the exception of semivoltinism (Fig. 4). The winter season (Bogan et al. 2013). However, flow was null model, which had no fixed effects predictor, was the observed in spring 2010 but absent in the spring of 2011 top model in predicting the relative frequencies of all trait and 2012. This suggests significant inter-annual variability modalities except semivoltinism; the Akaike weight (w) in stream flow; a pattern supported by Jaeger and Olden indicated high confidence this was true (w = 0.93–0.99) (2012). Large variation in seasonal flow intermittency (Table 3). Semivoltinism was the only trait modality that across the landscape had profound impacts on community could be predicted by microhabitat. Riffle samples had a assembly as demonstrated in seasonal patterns of taxa rich- higher proportion of semivoltine taxa compared to pool ness and trait composition. 2 samples but this effect was modest (Rm = 0.10). Macroinvertebrate taxa richness varied as a function of Analyzing both perennial and intermittent communi- hydrology, season, and microhabitat. Our first prediction ties in tandem revealed that hydrology was most important regarding the effect of hydrology on taxa richness was sup- in driving variation in the proportion of trait modalities. ported. As expected, at both individual microhabitat and Hydrology was the only predictor present in top models reach scales, perennial communities supported more taxa (Table 4). Intermittent communities supported dispropor- than intermittent communities did in all seasons. Factors 2 tionately more small-sized taxa (w = 0.97; Rm = 0.43) but that could have contributed to higher richness in perennial 2 fewer medium (w = 0.98; Rm = 0.34) and large-sized taxa reaches include increased habitat connectivity which pro- 2 (w = 0.85; Rm = 0.18) (Fig. 5). Taxa in intermittent streams motes transportation of resources and taxa dispersal (Ward were also more likely to possess the ability to undergo dia- et al. 1999), habitat stability (Death and Winterbourne 2 pause (w = 0.94; Rm = 0.34), and were less likely semi- 1995), increased size and diversity of habitats (Bonada 2 voltine (w = 0.57; Rm = 0 .16). Dispersal strategy, univol- et al. 2007), and a greater input of allochthonous resources tinism, and multivoltinism did not appear to be associated (Vannote et al. 1980). with hydrology, season, or microhabitat; the null model Our second prediction was supported in part; taxa was chosen to be the top model for these trait modalities. richness exhibited greater seasonal variability in intermittent streams (Fig. 2). With continuous year-round flow, perennial streams provide temporally stable habitats, thus Discussion maintaining relatively consistent taxa richness across seasons in comparison to intermittent streams. However, How communities assemble over time and across space contrary to our expectation, taxa richness peaked in fall remains a fundamental question in aquatic ecology. This and was lowest in spring in both perennial and intermit- question is especially relevant to dryland streams, which tent reaches. We predicted richness to be relatively high are characterized by heterogeneous flow regimes that lead in early spring owing to increased baseflow immediately to considerable spatiotemporal variability in habitat avail- after the traditionally wet winter season (Bogan et al. ability and condition. Over the 4-year duration of our study, 2013). Flow sensors deployed in intermittent streams

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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 different seasons. Trait modalities are Sm (small size), Md (medium size), Lg (large size), Dp (ability to diapause), NDp (no diapause), 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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Table 4 Coefficients of top-ranked linear mixed models (LMMs) that relates proportional trait richness among perennial and intermittent streams to hydrology (H), microhabitat (M), season (S), and their interactions

2 Traits Model w R m 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

w Akaike weight, i.e., the probability of the model being the best 2 among candidate models; R m proportional variance explained by fixed effects; Hint coefficient value for intermittent hydrology Microhabitat, season, and interaction terms were not included in the top-ranked models

from 2009 to 2011 found that flow remained intermit- Fig. 4 Mean proportion of trait modalities in reach-scale commu- tent in winter (Schriever et al. 2015), which might help nities in perennial a pools and b riffles across seasons. Error bars account for our results. Frequent stream drying events in reflect standard errors. Data include all sampling occasions intermittent stream reaches during winter likely acted as a strong habitat filter by removing taxa that could not survive 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- Table 3 Coefficients of top-ranked (ΔAICc <2) linear mixed mod- tion of the dry season (between late April and the mon- els (LMMs) that relate proportional trait richness within perennial reaches to season (S), microhabitat (M), and their interaction soon season starting in July) might have also contributed to lower taxa richness in intermittent reaches in spring. w R2 M Traits Model m rf Conversely, summer monsoon floods likely enhanced Body size connectivity between the perennial upstream and inter- Small ~1 0.99 0 mittent downstream reaches, thus allowing for increased Medium ~1 0.98 0 taxa dispersal and colonization. Further, Bogan and Large ~1 0.99 0 Boersma (2012) found that monsoon storms are a cue for Ability to diapause aerial dispersal of some invertebrates. The higher rich- Yes ~1 0.98 0 ness in fall relative to summer might also be reflective of Dispersal strategy the amount of time available for dispersal and coloniza- Aerial ~1 0.97 0 tion since the stream rewetted from monsoon runoff. Voltinism Microhabitat type played an important role in shaping Semivoltine ~M 0.99 0.10 0.03 diversity patterns. Pools supported higher taxa richness Univoltine ~1 0.93 0 than riffles in our dryland stream system. By contrast, pre- Multivoltine ~1 0.93 0 vious studies in other (non-dryland) stream systems did not find a consistent effect of microhabitat on richness (e.g., w Akaike weight, i.e., the probability of the model being the best 2 Logan and Brooker 1983; Boulton and Lake 1992; Carter among candidate models; R m variance explained by fixed effects; Mrf coefficient value for riffle microhabitat and Fend 2001; Bonada et al. 2006). The higher stabil- Hydrology, season, and interaction terms were not included in the ity of pools might have contributed to higher taxa rich- top-ranked models ness (Boulton and Lake 1992). However, the difference in

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Fig. 5 Mean proportion of trait modalities in reach-scale commu- errors. Data include only sampling occasions in which both perennial nities in a perennial pools, b intermittent pools, c perennial riffles, and intermittent habitats were available and d intermittent riffles across seasons.Error bars reflect standard taxa richness might also reflect the difference in sampling dry seasons and drought years (Bogan et al. 2013), allow- techniques between the microhabitats that was necessary ing for rapid colonization of existing habitat or dispersal to to obtain representative samples. Despite potential issues other intermittent reaches upon flow resumption. Riffles in in comparability of richness between microhabitats, the perennial reaches appeared to be modestly associated with effects of hydrology and season (as presented above) are semivoltine taxa; inspection of community data indicated robust because models controlled for microhabitat type. that riffle beetle (Heterelmis sp.—Family Elmidae) and a We observed clear differences in functional (trait) com- caddisfly taxon (Wormaldia sp.—Family Philopotamidae), position between communities in intermittent versus per- which are semivoltine, were common in riffles and thus ennial reaches, a finding that was consistent with our third contributed to this relationship. Whereas trait composition prediction. Intermittent reaches were characterized by hav- did not appear to vary in a consistent manner between sea- ing a greater fraction of taxa with small body size, ability sons among perennial streams, intermittent communities to undergo diapause, and uni- and multivoltinism. These in spring appeared to support a higher fraction of aerial traits impart resilience and/or resistance to temporally vary- dispersers than in other seasons (Fig. 5). This result is in ing stream conditions in line with predictions of the habitat partial agreement with our predictions regarding dispersal templet (Townsend and Hildrew 1994; Schriever and Lytle strategy (Table 1). Aerial dispersers were more numerous 2016). Taxa with small size and multivoltine life-cycles are in spring and only among intermittent streams because high classic r-strategists (MacArthur and Wilson 1967) whose flow intermittency in winter-early spring likely impeded rapid growth rates, short life spans, and relatively high aquatic dispersal. By contrast, year-round habitat availabil- fecundity allow timely reproduction before stream dry- ity in perennial reaches would not have selectively favored ing and quick colonization once intermittent stream flow taxa with traits that confer an advantage in highly variable resumes. Similarly, the ability to survive dry conditions environments. in one or more life-stages allows taxa to persist in situ in

1 3 715 Hydrology drives seasonal variation in dryland stream macroinvertebrate communities

By modelling patterns in trait modality we strengthened With climate change and increasing human water the inferences drawn from the multivariate analysis. Across abstraction, an increasing number of perennial streams in all stream reaches, hydrology was the most important vari- dryland stream systems are projected to become intermit- able in predicting the proportion of macroinvertebrate com- tent (Larned et al. 2010) including the ones studied here munities characterized by taxa in various size categories, (Seager et al. 2013; Jaeger et al. 2014). Mediterranean ability to diapause, and voltinism. This suggests consider- stream systems are expected to experience drier condi- able species sorting based on functional trait adaptations to tions and an increased number of droughts, thus resem- flow intermittency, and that mass effects exerted relatively bling dryland streams (Filipe et al. 2013). By characteriz- little influence on species communities. If mass effects ing changes in aquatic macroinvertebrate communities in were more important, we would expect passive dispersal different microhabitats within perennial and intermittent to dilute differences in trait composition between perennial reaches across seasons in multiple years, our study pro- and intermittent sites once flow resumes in the latter habi- vides an indication of how these communities in dryland tat. Moreover, we did not detect a hydrology-season inter- and Mediterranean stream systems may respond to climate action, which would be expected if trait composition in per- change and increased human water use. Taxa richness at ennial and intermittent communities homogenized in the both microhabitat and reach scales are expected to decline summer monsoon season (when intermittent reaches first across all seasons, and seasonal richness differences would reconnect to upstream perennial reaches) before diverging likely become more pronounced as more dryland stream in fall as flow stabilized and communities equilibrated. reaches transition from perennial to intermittent flow, and Among perennial reaches, the proportion of taxa in as Mediterranean-climate streams experience more dry- all trait modalities, with the exception of semivoltinism, land-like conditions. We expect changes in taxa richness to were similar across seasons and between habitats, sug- be accompanied by an increase in the proportion of small- gesting considerable spatiotemporal homogeneity in func- bodied taxa, multivoltine taxa, and taxa that possess the tional composition. Riffles were weakly correlated with an ability to undergo diapause. Given the prospect of losing increase in the fraction of semivoltine taxa, supporting our taxonomic and trait diversity, further long-term research is conclusions from the NMDS analysis. We did not formally required to not just document these potential changes, but model seasonal effects among intermittent reaches because also understand their effects on stream ecosystem function. we had few replicates across seasons, which reflected the unpredictability of flow in intermittent reaches of dryland Acknowledgements Funding was provided by the US Department of Defense (SERDP RC-1724, RC-2203, RC-2511). We thank Sheri- stream systems. We were thus unable to confirm the effect dan Stone for logistical support at Fort Huachuca, and Brooke Gebow of season on dispersal strategy (as inferred from the NMDS and the Nature Conservancy for access to streams and lodging at the ordination) among intermittent streams. Ramsey Canyon Preserve, Arizona. This manuscript benefited from Traits associated with intermittent versus perennial the valuable comments of two anonymous reviewers. streams in our study were similar to those identified in Author contributions XG led writing of the manuscript. XG and the Mediterranean-climate streams in northeastern Spain WC analysed data. JDO and DAL designed study. DAL and TAS per- (Bonada et al. 2007). This indicates some generality in formed field work and collated trait data. RVD led taxonomic identifi- trait-environment relationships across streams in different cations. All authors contributed to the writing of the manuscript. climates. A formal meta-analysis that uses a single standardized framework to analyze multiple datasets (e.g., Datry et al. 2014; Leigh et al. 2016) could examine whether the References strength of these relationships differ across latitudinal or flow permanence gradient. Whereas Bêche et al. (2006) Acuña VM, Muñoz I, Giorgi A, Omella M, Sabater F, Sabater S found clear seasonal variation in trait composition in both (2005) Drought and postdrought recovery cycles in an intermit- perennial and intermittent Mediterranean-climate streams tent Mediterranean stream: structural and functional aspects. J N Am Benthol Soc 24:919–933 in California, there was little indication that season affected Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Sing- trait composition of perennial reaches in our study. Differ- mann H, Dai B, Grothendieck G, Green P (2016) lme4: linear ences in seasonality in rainfall and thus flow could partially mixed-effects models using ‘Eigen’ and S4, 1.1–12.https:// explain the discrepancy; the Mediterranean-climate streams cran.r-project.org/web/packages/lme4/index.html. Accessed Sept 2016 studied by Bêche et al. (2006) had a longer winter wet sea- Bêche LA, McElravy EP, Resh VH (2006) Long-term seasonal son (from November to May) and lacked the summer mon- variation in the biological traits of benthic-macroinvertebrates soon observed in our dryland streams. The lower annual in two Mediterranean-climate streams in California, U.S.A. rainfall in dryland streams might have also imposed a strict Freshw Biol 51:56–75 Bogan MT, Boersma KS (2012) Aerial dispersal of aquatic inver- habitat filter at the landscape level, resulting in lower sea- tebrates along and away from arid-land streams. Freshw Sci sonal trait variation. 31:1131–1144

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