Dynamics of ground-dwelling arthropod metacommunities in intermittent streams: The key role of dry riverbeds

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Dynamics of ground-dwelling arthropod metacommunities in intermittent streams: The key role of dry riverbeds María Mar Sánchez-Montoyaa,b, , Klement Tocknerb,c,1, Daniel von Schillerd, Jesús Miñanoa, Chema Catarineue, Jose L. Lencinaf, Gonzalo G. Barberág, Albert Ruhih ⁎

a

Department of Ecology and Hydrology, Regional Campus of International Excellence Campus Mare Nostrum-University of Murcia, Campus de Espinardo, Murcia, Spain Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), 12587 Berlin, Germany c Institute of Biology, Freie Universität, 14195 Berlin, Germany d Department of Plant Biology and Ecology, Faculty of Science and Technology, University of the Basque Country (UPV/EHU), Bilbao, Spain e Asociación de Naturalistas del Sureste (ANSE), Murcia, Spain f Sanidad Agrícola Econex S.L., Spain g Department of Soil and Water Conservation, CSIC-CEBAS, Campus Universitario de Espinardo, Murcia, Spain h Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, CA 94720, USA b

ARTICLE INFO

ABSTRACT

Keywords: Biodiversity conservation Beta diversity Drought Ground-dwelling arthropods Mediterranean-climate streams

Intermittent streams are subject to high levels of environmental variation. However, little is known about how biota responds to river drying across the channel-to-upland habitat gradient. This is an important shortcoming because assumes that intermittent river habitats and metacommunities are static. Here we studied how river drying affects the spatial and temporal variation in ground-dwelling arthropod communities (spiders, beetles, and ants) across the lateral habitat gradient. We asked whether particular habitats, moments, or species contribute disproportionally to beta diversity. To this end, we monitored two perennial-intermittent reach pairs during an entire drying cycle, and applied beta-diversity partitioning methods to highly-resolved taxonomy data. We predicted that: (i) intermittent reaches would accumulate higher levels of diversity (alpha and beta) than perennial reaches; (ii) dry riverbeds would harbor more species and more unique species; (iii) alpha and beta diversity would be temporally more variable in intermittent than in permanent reaches; and (iv) species dispersal limitation would explain variation in contributions to beta diversity. Intermittent reaches presented higher alpha and beta diversity, with dry channels harboring more unique species and more species than any other habitat. Arthropod metacommunities were more variable across space than over time, and temporal turnover was significant—with species dispersal limitation being positively associated with contributions to beta diversity. Our results elevate the role of dry channels in intermittent river ecology, and show that previous research has likely underestimated their contributions to river-wide biodiversity. Our findings call for the need to integrate the dry phase of intermittent streams into monitoring and conservation programs.

1. Introduction Rivers create lateral habitat gradients (e.g. Naiman and Decamps, 1997; Nakano and Murakami, 2001; Muehlbauer et al., 2014) that shape plant and animal biodiversity along the river corridor (e.g. Sabo et al., 2005; Biswas and Mallik, 2010; Soykan et al., 2012). This habitat gradient is influenced by hydrologic processes that originate in the channel—periodic flood and drought disturbances that affect the physical habitat, biota, and their interactions (Ward et al., 2002; Power

et al., 2008; Palmer and Ruhi, 2019). This is particularly true in intermittent rivers, where flow intermittency generates a dynamic mosaic of lotic (flowing water), lentic (standing water), and terrestrial habitats (dry riverbed) (Datry et al., 2016). The physical process of dry-rewetting sequences triggers complex species dispersal and colonization cycles (Sánchez-Montoya et al., 2016a), influencing the dynamics of whole animal assemblages (Ruhi et al., 2017; Sarremejane et al., 2017). As a result, intermittent rivers support not only aquatic fauna, but also diverse and abundant terrestrial and semiaquatic organisms during

Corresponding author at: Department of Ecology and Hydrology, Regional Campus of International Excellence Campus Mare Nostrum-University of Murcia, Campus de Espinardo, Murcia, Spain. E-mail address: [email protected] (M.M. Sánchez-Montoya). 1 Current address: Austrian Science Fund, 1090 Vienna, Austria. ⁎

https://doi.org/10.1016/j.biocon.2019.108328 Received 29 March 2019; Received in revised form 29 October 2019; Accepted 1 November 2019 0006-3207/ © 2019 Elsevier Ltd. All rights reserved.

Please cite this article as: María Mar Sánchez-Montoya, et al., Biological Conservation, https://doi.org/10.1016/j.biocon.2019.108328

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both the wet and dry phases (Steward et al., 2017; Sánchez-Montoya et al., 2017). However, research to date has largely focused on aquatic organisms and the wet phase (Skoulikidis et al., 2017). Understanding the ecological processes that take place during the dry phase thus remains a critical gap in intermittent river ecology. Terrestrial arthropods are also structured along the riparian-upland habitat gradient (Soykan et al., 2012), where they play essential ecological roles, influencing nutrient cycling, plant productivity, and the abundance of other invertebrates and vertebrates (Price, 1984). Evidence suggests that dry riverbeds may support diverse arthropod assemblages (e.g. Wishart, 2000; Steward et al., 2011; Corti and Datry, 2016; Sánchez-Montoya et al., 2016a). These communities can be a subset of those found in the fringing terrestrial habitat assemblage (Corti and Datry, 2016); however, species turnover is in some cases very high—with shared species representing only around 20% of the pool (Steward et al., 2011). Because flow intermittency is expected to increase as a consequence of the combined effects of climate change, land-use change, and human overallocation of water resources (Larned et al., 2010; Döll and Schmied, 2012; Datry et al., 2014), quantifying the contributions of these habitats to river-wide biodiversity has profound implications for conservation. Analyses of species contributions to community diversity over space and time can help determining the role of spatial and environmental processes in structuring metacommunities, or sets of local communities potentially linked by dispersal (Leibold et al., 2004). For example, wetdry cycles may constrain the movement of species with limited dispersal, thus increasing dissimilarity in community composition across locales (Landeiro et al., 2018). Determining how particular habitats (space) and moments (time) contribute to metacommunity diversity may also support the development of effective conservation strategies in dynamic river corridors (Ruhi et al., 2017). This rationale was applied effectively decades ago to promote conservation efforts in riparian habitats. Riparian habitats tend to harbor more species than nearby upland areas (Naiman et al., 1993; Whitaker et al., 2000), an observation that is often attributed to their high productivity (Naiman and Decamps, 1997). Riparian habitats also harbor unique sets of species, thus enriching the regional species pool (Sabo et al., 2005; Soykan et al., 2012). While these observations motivated the inclusion of riparian zones as priority habitats in conservation planning (e.g. Clerici and Vogt, 2013), they could apply to dry riverbeds if evidence supported the ecological uniqueness of these habitats. In this study, we examined the effects of river drying on terrestrial arthropod assemblages along lateral aquatic-terrestrial gradients (i.e. channel, riparian, and upland habitats). We compared alpha and beta diversity patterns of ground-dwelling arthropods in wet-dry channel pairs along two Mediterranean streams during an entire dry phase. We identified ‘keystone’ habitats and moments (i.e. sites and times supporting disproportionally high levels of alpha and beta diversity; sensu Mouquet et al., 2013), as well as species that contribute to ecological uniqueness (sensu Landeiro et al., 2018). Leveraging the range of dispersal abilities of arthropods and their variety of responses to landscape properties (Adis and Junk, 2002; Schaffers et al., 2008), we selected three arthropod groups that are abundant along intermittent river corridors as well as in the fringing upland habitats: spiders, ants, and beetles (e.g. Sánchez-Montoya et al., 2016a). We hypothesized that drying and subsequent secondary succession in dry riverbeds (i.e. availability of competitor- and predator-free habitat rich in resources; Connell and Slatyer, 1977) would increase spatial and temporal variation in community composition. In agreement with recent work (Sánchez-Montoya et al., 2016a), we anticipated that dry riverbeds would play an important – yet still unrecognized – role in promoting community reassembly (Fig. 1). In particular, we predicted that: (i) intermittent reaches would accumulate higher levels of diversity (alpha and beta) than perennial reaches, given the higher levels of environmental variation of habitats that undergo wet-dry cycles; (ii) dry riverbeds would act as keystone habitats across lateral

gradients (i.e. channel-to-upland), by harboring more species and more unique species; (iii) alpha and beta diversity would be more temporally variable in intermittent than in permanent reaches; and (iv) species dispersal limitation and Species Contributions to Beta Diversity would be positively associated, as highly-mobile species connect multiple habitats and thus homogenize species composition across the landscape. 2. Methods 2.1. Study area and sampling sites This study was developed in two intermittent headwater streams: Fuirosos (Fui; 8 km long; 15.2 km2) and Rogativa (Rog: 16 km long; 47.2 km2), located in northeastern and southeastern Spain respectively (Fig. 2). Both catchments are subject to low human pressure (natural land cover > 90%) and are part of protected areas. Despite being classified as warm temperate areas (Csa Köppen-Geiger climate type; Rubel et al., 2017), Fuirosos is colder (mean annual temperature: Fui = 13.3 °C; Rog = 14.3 °C), wetter (mean annual rainfall: Fui = 750 mm; Rog = 583 mm), and has a more predictable flow regime than Rogativa (Fig. 2). Both streams have spatially and temporally intermittent flow regimes (see Sánchez-Montoya et al., 2018). In Fuirosos, riparian and upland areas are densely covered by vegetation (riparian habitat: helophytes, grasses, alder, and hazelnut; upland habitat: mainly pine and holm oak); in Rogativa, vegetation is scarcer (riparian habitat: helophytes; upland habitat: shrubs and pines). In both streams the channel has a similar width (~3 m wide). A detailed description of the study sites is provided in Sánchez-Montoya et al. (2016a). 2.2. Experimental design and sample collection Along each stream corridor we selected two 80-m-long reaches (one perennial, one intermittent) representative of the catchment. Study reaches were located about 3 km apart, and were characterized by wellpreserved riparian and upland habitats. They also exhibited similar channel characteristics (i.e. width, topography, substrate composition). In all four study reaches we collected ground-dwelling arthropods in July and August of 2013, on five sampling dates spanning 2, 4, 10, 15, and 29 days after complete surface drying (which started about the same time in both streams). Three transects, located 40 m apart and perpendicular to the channel, were established in each reach. Along each transect, three habitat types were sampled: channel, riparian, and upland. Channels were sampled in the center of the dry stream (for intermittent reaches), and in exposed sediments a few centimeters from the edge of surface flow (for perennial reaches). Riparian habitats, characterized by a different plant composition from the uplands, were sampled in their central section. Finally, upland habitats in both reach types were sampled at a distance of about 50 m from the stream channel's edge. Five pitfall traps, located 1 m apart from each other, were deployed on each sampled habitat for 48 h (N = 900). This method is commonly used for cursorial arthropods that are active on the soil surface, such as spiders, beetles, and ants (e.g. Ellis et al., 2001). Each pitfall trap consisted of two plastic containers (height: 80 mm, diameter: 80 mm), one inside the other and set into the ground (the inner cup could be removed to collect specimens, while the outer cup was permanent). The inner cup was filled with water, salt (as preservative), and detergent (to lower surface tension and prevent captured invertebrates from escaping). In the laboratory all terrestrial invertebrates belonging to the orders Araneae (spiders) and Coleoptera (beetles), and to the family Formicidae (ants), were counted and identified to the species level. These three taxonomic groups, together with Collembola, dominated the terrestrial assemblages in the study area (Sánchez-Montoya et al., 2016a). 2

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Intermittent reach

Perennial reach

Channel Riparian

Upland

LC

=6 =0.42 LC

=5 =0.30 LC

=3 =0.27

LC

=8 =0.44 LC

=5 =0.30 LC

=3 =0.27

Channel Riparian

Upland

LC

=6 =0.42 LC

=5 =0.30 LC

=3 =0.27

LC

=7 =0.42 LC

=5 =0.30 LC

=3 =0.27

Fig. 1. Conceptual diagram summarizing expected changes in alpha and beta diversity over space and time in an intermittent vs. a perennial stream reach. White circles represent local communities; symbols represent species within a local community. Secondary succession, and environmental filtering by drying, explains general patterns in alpha and beta diversity in intermittent streams. In particular, we predict that: (i) Spatial variation of alpha and beta diversity in habitats along the lateral gradient will be stronger in intermittent than perennial reaches; (ii) temporal variation of alpha and beta diversity will be higher in intermittent relative to perennial reaches, as a consequence of their changing environmental conditions across the dry period; and (iii) at the end of dry period, alpha diversity in dry channels will decline as a consequence of increasing competition for space and resources.

2.3. Statistical analysis

Hellinger-transforming abundance data. Second, we used Generalized Least Squares Models to evaluate the effects of flow type (perennial vs. intermittent), habitat type (channel, riparian, upland), date (day: 2, 4, 10, 15, 29) and transect (1, 2, 3) on alpha diversity and LCBD. We again explored these relationships for each group (spiders, ants, and beetles) and for the entire assemblage. We constructed three different models (Table S1). Model 1 considered all factors but no interactions. Model 2 included a Flow × Habitat interaction, which allows for habitat gradients to affect diversity in different ways in perennial vs. intermittent reaches. Finally, Model 3 was the most complex and included a triple Flow × Habitat × Date interaction—meaning that the interaction considered in the previous model was in turn dependent on day after flow cessation. All models included a compound symmetry covariance structure, with samples collected within the same site, habitat, transect, and date, falling within the same grouping level. We tested model diagnostics and examined residuals for normality and temporal autocorrelation, using the autocorrelation function (ACF). We contrasted models via information-theoretic model comparison, using the Akaike Information Criterion (AIC) (Burnham and Anderson, 2003). Finally, we asked whether species contributing more to beta diversity were more likely to be dispersal limited. All species were classified as strong or weak contributors to beta diversity depending on their SCBD values (i.e., higher or lower than the community average). In addition, species were assigned to two dispersal categories (strong and weak dispersers; Table S2). For spiders, we classified families into

First, we calculated alpha and total beta diversity, as well as the relative importance of the two components of beta diversity (i.e. richness and replacement; Baselga, 2010; Legendre, 2014). We computed these metrics in each reach separately, by pooling data from the different transects within each habitat and date. Thus, these metrics represent both spatial and temporal variation in composition. We followed this procedure for each taxonomic group, and then for the three groups combined (hereafter ‘entire assemblage’). We estimated beta diversity via Jaccard-based indices of the Podani family, and we partitioned the richness and replacement components using the ‘beta.div.comp’ function available in the ‘adespatial’ R package (Legendre, 2014; Dray et al., 2016). In addition, we calculated Local Contribution to Beta Diversity (LCBD) and Species Contribution to Beta Diversity (SCBD) for each study stream, both for each taxonomic group and for the entire assemblage. LCBD provides a measure of the relative contribution of a given sampling unit to beta diversity; in our case, that measure represents the ecological uniqueness of a study habitat (i.e. an ‘unusual’ combination of species). In turn, SCBD measures the contribution that individual species make to overall beta diversity, with high SCBD values identifying unique species (i.e. species present in an ‘unusual’ combination of sites). For both LCBD and SCBD, higher values reflect higher contributions to overall beta diversity, and thus higherthan-average conservation scope (Landeiro et al., 2018). We calculated both metrics following Legendre and De Cáceres (2013), after 3

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Fig. 2. Location of the study basins and sites in the Iberian Peninsula (left), and summary of their respective hydrologic regimes (right). The wavelet power spectra on 60-yr monthly rainfall data shows that environmental predictability (i.e., seasonality, or variation in rainfall explained by periodic, 6-month cycles) is higher in Fuirosos than in Rogativa. Red dots identify statistically-significant periodicities (tested against a null model of red noise).

sedentary (weak dispersers) and wandering species (strong dispersers), according to Wise (1995), considering weaver and burrowing spiders in the former group, and the rest of hunter species in the latter group. Guild categories were obtained from Cardoso et al. (2011). For ants, we focused on the seed dispersing genera, with individual species being categorized as strong or weak dispersers based on reported dispersal distances (Gómez and Espadaler, 2013) relative to the community mean. For beetles, we classified species as strong or weak dispersers depending on whether they could fly (winged and wingless species, respectively). In this paper, we use wingless beetles to refer to all species that have lost the ability to fly, even if they possess reduced wings. We then conducted a Chi-square independence test to determine whether an association existed between SCBD and dispersal abilities within each group.

Table 1 Alpha diversity and Total Beta diversity and its components (Replacement and Richness) for intermittent and perennial reaches in the two study streams (Fuirosos and Rogativa), for the entire assemblage and for each group (‘Spiders’, ‘Ants’, ‘Beetles’). Alpha diversity

3. Results 3.1. General patterns of alpha and beta diversity A total of 270 arthropod species (i.e. spiders, ants, beetles) were recorded in the two streams over the entire study period (Table S2). Samples collected in Rogativa contained a higher number of arthropod species than samples collected in Fuirosos (Fui: 112 spp.; Rog: 164 spp.). Beetles were the most diverse group in Fuirosos (Fui: 52 spp.; Rog: 63 spp.), spiders in Rogativa (Fui: 40 spp.; Rog: 68 spp.), followed by ants in both streams (Fui: 20 spp.; Rog: 33 spp.). As expected, both alpha and beta diversity values were generally higher in intermittent compared to perennial reaches (Table 1), except for spider alpha diversity, and spider and beetle beta diversity (Rogativa). The replacement component of beta diversity prevailed over the richness component, meaning that variation in species identities structured metacommunities to a higher degree than variation in species pools (Table 1).

Total Beta diversity

Replacement/ Total Beta diversity

Richness/ Total Beta diversity

Entire assemblage Spiders Ants Beetles

Fuirosos Perennial 59 0.364 22 0.351 7 0.260 30 0.260

0.714 0.634 0.418 0.418

0.286 0.366 0.582 0.582

Entire assemblage Spiders Ants Beetles

Fuirosos Intermittent 94 0.389 38 0.379 18 0.354 38 0.428

0.581 0.501 0.676 0.474

0.419 0.499 0.324 0.526

Entire assemblage Spiders Ants Beetles

Rogativa Perennial 114 0.351 55 0.399 23 0.221 36 0.485

0.703 0.747 0.510 0.514

0.297 0.253 0.490 0.486

Entire assemblage Spiders Ants Beetles

Rogativa Intermittent 128 0.355 52 0.385 30 0.247 46 0.470

0.604 0.644 0.549 0.524

0.396 0.356 0.451 0.476

3.2. Spatial variation in the metacommunity For the entire arthropod assemblage, and the three taxonomic groups individually, dry channels were more diverse than all other habitat types, with alpha diversity decreasing along the channel-to4

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Fuirosos

Alpha diversity (entire assemblage)

30

Rogativa

Model 2: F, H, D, FxH

Model 2: F, H, D, FxH

20

10

0

LCBD (entire assemblage)

0.06

0.04

0.02

0

Model 1: F, H, D Intermittent

Model 2: F, H, D, FxH

Perennial

Intermittent

Perennial

Fig. 3. Alpha diversity and Local Contribution to Beta Diversity (LCBD) for the entire assemblage, in the three study habitats (channel: blue color; riparian: green color; upland: brown color), two reaches (perennial and intermittent), and two streams (Fuirosos and Rogativa). The central bar of each violin plot indicates the mean value. The best supported model structure (selected via AIC) is shown, with red fonts denoting significant (p < 0.05) effects (see text for details). F = flow type (intermittent vs. perennial); H = habitat type (upland, riparian, channel); D = date (day: 2, 4, 10, 15 and 29).

upland gradient (Figs. 3, S1–S3). This was the case in both rivers (all reaches), and particularly pronounced along intermittent reaches. Significant Flow × Habitat interactions occurred in five out of eight cases (Tables S3–S6). In Fuirosos, dry channels exhibited a higher Local Contribution to Beta Diversity (LCBD) than all other habitat types (both perennial and intermittent reaches), except for beetles (Figs. 3, S1–S3). However, in Rogativa this pattern only occurred for beetles. Flow × Habitat interactions were significant only in Fuirosos (for spiders and ants; Tables S3–S6).

to overall beta diversity (SCBD > 0.20) (Table 2). In Fuirosos, the four ant species presented higher SCBD values than the six spider and two beetle species. Similarly, in Rogativa seven out of 10 ant species contributed higher than the two spider species. Those species showed different affinities for flow regime and habitat types (Table 2). In all cases except for spiders in Rogativa, associations between dispersal abilities and SCBD were inverse (i.e., the lower the dispersal abilities, the higher the contribution to beta diversity) (Fig. 5). Associations were significant for spiders in Rogativa (Fui: χ2 = 0.637, p = 0.727; Rog: χ2 = 5.802, p = 0.016), for ants in Fuirosos (Fui: χ2 = 4.444, p = 0.035; Rog: χ2 = 0.055, p = 0.814), and for beetles in both streams (Fui: χ2 = 6.405, p = 0.011; Rog: χ2 = 53.788, p = 0.047).

3.3. Temporal variation in the metacommunity As predicted, alpha diversity fluctuated more in intermittent than in perennial reaches (both streams, entire assemblage and most groups; Figs. 4, S4–S6). However, fluctuations were not spatially synchronous: in the intermittent reaches (both rivers), opposite trajectories occurred between dry channels and adjacent terrestrial habitats (Fig. 4). Date was a significant factor only in Rogativa (entire assemblage and ants; Tables S3–S6). LCBD exhibited a higher temporal variation in intermittent than in perennial reaches in Fuirosos, except for beetles. In Fuirosos, the higher LCBD of dry channels was maintained or even increased during the dry period, except for beetles lacking a clear pattern. Date was a significant factor only for entire assemblage and ants in Fuirosos.

4. Discussion In this study we analyzed the effects of river drying on the spatial and temporal variation of terrestrial invertebrate diversity (alpha and beta) across lateral, channel-to-upland gradients. This allowed identifying key habitats, moments, and species contributing to diversity in intermittent relative to perennial streams. We had predicted that channel drying triggers secondary succession in intermittent rivers, leading to higher levels of diversity in intermittent than in perennial reaches. As predicted, dry riverbeds contained more species, and more unique species than riparian and upland habitats. We also had predicted that alpha and beta diversity would be temporally more variable in intermittent than in permanent reaches, and that dispersal limitation would be positively associated with the contribution that particular species make to beta diversity. Our results confirm, in general, these predictions, as further discussed below. Overall, our findings suggest

3.4. Dispersal limitation and contributions to beta diversity Particular species in all three groups contributed disproportionately 5

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Alpha diversity (entire assemblage) Rogativa Fuirosos

Intermittent

across-habitat community reassembly in intermittent streams. As predicted, arthropod diversity was higher in dry channels than in all other habitats, including flowing channels and riparian zones. This finding is interesting because it contrasts with abundant research on the aquatic phase showing that intermittent habitats tend to be speciespoorer, across climates and biological groups—particularly for arthropods (Leigh and Datry, 2017; Soria et al., 2017). The higher diversity we found is most likely a consequence of the distinct secondary succession (sensu Connell and Slatyer, 1977) initiated by surface drying—a process that does not have a parallel over the wet phase. At the onset of the dry phase, channels provide competitor-predator free space, as well as abundant unexploited resources. Although it is often assumed that surface flow drying may enable the colonization of the stream bed by invertebrates seeking stranded aquatic organisms and other subsidies (e.g. Larimore et al., 1959; Lake, 2003), very little empirical evidence of this phenomenon exists. This may indicate that different resources along the lateral gradient may influence local community composition, with dispersal allowing species to track changes in environmental conditions in dry channels, as described by the species-sorting metacommunity paradigm (Leibold et al., 2004). As observed in Fuirosos (but not in Rogativa), dry channels can increase regional species richness by harboring different and more species—in contrast to what has been observed from riparian habitats, which increase regional richness by harboring different (but not more) species (Sabo et al., 2005; Steward et al., 2011). Dry channels may also be used by fauna to disperse, reproduce, and protect from predation or harsh environmental conditions (Sánchez-Montoya et al., 2016b, 2017; Steward et al., 2018). Although dry channels have been traditionally considered harsh environments because the lack of vegetation increases exposure to solar radiation and wind (Steward et al., 2011), SánchezMontoya et al. (2016a) showed that these habitats hosted a higher abundance and richness (at a coarse taxonomic resolution) of grounddwelling arthropods than their perennial counterparts and the fringing terrestrial habitats. These previous observations, combined with the results reported here, warrant further investigation of the key ecological functions provided by dry riverbeds (see Steward et al., 2012). Our study also found that temporal variation in alpha diversity was higher in intermittent than in perennial reaches, supporting the notion that the temporal dimension of variation may be an important, yet overlooked aspect of empirical metacommunity studies in rivers (Sarremejane et al., 2017; Ruhi et al., 2017, 2018). Interestingly, alpha diversity peaked at the onset (first 10 days) of the dry phase and decreased afterwards, probably reflecting increasing competition for space and resources, consistent with secondary succession patterns (e.g. Cook et al., 2005). Although the current study focused on spiders, ants, and beetles, these three taxonomic group dominated the terrestrial assemblages, accounting for 77% of individuals (data of both streams combined; see Sánchez-Montoya et al., 2016a). Thus, these groups likely capture assemblage-level patterns. Dispersal plays a dominant role in all four metacommunity perspectives that are frequently identified (i.e. species sorting, mass effects, patch dynamics, and neutral) (Leibold et al., 2004). In our study we observed an association between SCBD and dispersal limitation, with weak dispersers diversifying local communities across the landscape, as previously reported of stream aquatic insects (e.g. Heino and Grönroos, 2017). Ants contributed highly to beta diversity, which could be explained by the high dispersal constraints faced by this group compared to spiders and beetles. This pattern is probably due to the strong dependence of ants on their nests (Hölldbler and Wilson, 1990). In fact, the six species with highest SCBD values (> 0.060) are myrmicine ants characterized by a sedentary behavior with fixed nest sites and very low dispersal distances (< 2 m; Gómez and Espadaler, 2013). Overall, our results suggest that intermittent river biodiversity may be maintained by both environmental filtering processes (shown by a combination of high LCBD with low alpha richness; Legendre and De Cáceres, 2013; Landeiro et al., 2018) and by species dispersal limitation (shown by

Perennial Model 2: F, H, D, FxH Channel

30

Riparian Upland

20 10 0

Model 2: F, H, D, FxH 30 20 10 0

Model 1: F, H, D

Rogativa

LCBD (entire assemblage) Fuirosos

0.06

0.04 0.02 0

Model 2: F, H, D, FxH 0.06 0.04

0.02 0 2 4

10

15

29 2 4 10 Dry phase (days)

15

29

Fig. 4. Mean (+SD) of alpha diversity, and Local Contribution to Beta Diversity (LCBD) for the entire assemblage in the three study habitats (channel, riparian and upland), two reaches (perennial and intermittent), and two streams (Fuirosos and Rogativa streams) over the dry period. The best supported model structure (selected via AIC) is shown, with red fonts denoting significant (p < 0.05) effects (see text for details). F = flow type (intermittent vs. perennial); H = habitat type (upland, riparian, channel); D = date (day: 2, 4, 10, 15 and 29).

that dry channels play a key role in structuring intermittent river metacommunities, and call for conservation actions to be prioritized in these habitats. Although the effects of floods on the diversity of terrestrial arthropods in riparian and upland areas have received much attention (Ellis et al., 2001; Adis and Junk, 2002; Lambeets et al., 2008), information on the effects of river drying is much scarcer (see e.g. McCluney and Sabo, 2012; Corti and Datry, 2013). There is evidence that drying reduces the abundance of terrestrial riparian invertebrates by reducing their aquatic prey (Allen et al., 2014). However, recent comparisons of riparian communities along surface water permanence gradients revealed that arthropod diversity in riparian habitats fringing intermittent streams can be as high as along perennial streams, despite composition differing considerably (Moody and Sabo, 2016). We found that the dry phase may alter invertebrate diversity and composition not just in the channel and in riparian habitats, but also in the upland habitats—as shown by the higher alpha and beta diversity of grounddwelling arthropods in uplands along intermittent reaches. The dominance of replacement gradients in explaining beta diversity confirms that strong environmental gradients exist, and that the dry phase drives 6

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Table 2 Species contribution to beta diversity (in parentheses) for spiders, ants, and beetles in Fuirosos and Rogativa streams. Only species with values > 0.20 are shown. Abundances for each species along the study period are indicated (white cells = 0 individual; yellow = abundances < first quartile (1st Q); orange = abundances between 1st and 2nd Q; grey = abundances between 2nd and 3rd Q; black = abundances > 3rd Q) for both intermittent and perennial reaches.

Fuirosos Habitat

Tenuiphantes tenuis (0.056)

Channel

Pardosa hortensis (0.036)

Channel

Pardosa proxima (0.029)

Channel

Gongylidiellum vivum (0.028)

Channel

Saitis barbipes (0.025)

Channel

Eratigena fuesslini (0.023)

Channel

Lasius emarginatus (0.097)

Channel

Pheidole pallidula (0.072)

Channel

Aphaenogaster subterranea (0.063)

Channel

Crematogaster scutellaris (0.056)

Channel

Asida jurinei jurinei (0.058)

Channel

Acrotrichis fasciculatus (0.023)

Channel

D2

D4

D10

D15

Intermittent D29

D2

D4

D10

D15

Rogativa Species

D29

Riparian

Spiders

Species

Perennial

Upland Riparian

Perennial D2

D4

D10

D15

Intermittent D29

D2

D4

D10

D15

D29

Wadicosa fidelis (0.035) Pardosa cribrata (0.027)

Spiders

Upland Messor capitatus (0.083)

Riparian Upland

Tapinoma nigerrimum (0.076)

Riparian Upland

Lasius grandis (0.066)

Riparian Upland

Iberoformica subrufa (0.064)

Riparian Upland

Pheidole pallidula (0.048)

Riparian

Ants

Ants

Upland Riparian

Crematogaster auberti (0.046)

Upland Cataglyphis velox (0.039)

Riparian Upland

Tetramorium caespitum (0.026)

Riparian

Beetles

Upland Messor bouvieri (0.022)

Riparian Upland

Crematogaster sordidula (0.021)

Riparian Upland

high SCBD), which may prevent part of the assemblage from fully tracking spatio-temporal environmental variation. This study used highly-resolved (species-level) data to study the contributions made by different habitats and moments to river-wide biodiversity, and found that dry channels from intermittent rivers play a more important role for invertebrate metacommunities than previously assumed. Future studies should expand the gradient of drying harshness by incorporating intermittent rivers in other climates, and should test whether our inferences on arthropod metacommunity dynamics hold when studied over longer periods of time. If our findings are confirmed, the dry phase should become an integral part of intermittent stream biomonitoring programs. Recent studies have shown that terrestrial invertebrates are sensitive to anthropogenic pressures (Steward et al., 2018), in addition to being abundant in dry riverbeds. For these reasons they have been proposed as suitable indicators of dry riverbed health, similarly to aquatic macroinvertebrates used as bioindicators of river ecosystem integrity. Our results support further

investigation of the biomonitoring potential of terrestrial arthropods. However, they also suggest limited promise in using particular taxonomic groups as biodiversity surrogates, given the idiosyncratic responses to spatio-temporally variable conditions of intermittent rivers. 5. Conclusion Whereas dry riverbeds have been traditionally overlooked in both terrestrial and aquatic ecology research, this habitat disproportionally contributes to river corridor biodiversity. This observation supports the need to develop essential biodiversity variables that apply to these habitats, and that integrate both the dry and wet phases, and the whole lateral habitat continuum (Acuña et al., 2017). Intermittent rivers are consistently underrepresented in policy of frameworks (Acuña et al., 2014; Marshall et al., 2018), often owing to lower biodiversity values (relative to their perennial counterparts) and inconsistent valuation by the public (Acuña et al., 2017). We contend that an incorrect appraisal 7

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Fuirosos Spider

100% 100%

Ant *

Rogativa Beetle *

Spider *

Ant

Beetle *

100%

90%

90%

80% 80%

80%

70%

70%

60% 60%

60%

50%

50%

40% 40%

40%

30%

30%

20% 20%

20%

10%

10%

0% 0%

0% Low SCBD High Low SCBD Spider SCBD High SCBD

Low SCBD Low High SCBD Ant SCBD High SCBD

Strong dispersers

High SCBD Low SCBD Low High SCBDSpider SCBD

Low SCBD Low High SCBD Beetle SCBD High SCBD

Low SCBD High Low SCBD Ant SCBD

High SCBD

High SCBD Low SCBD High Low SCBDBeetle SCBD

Weak dispersers

Fig. 5. Association between organismal dispersal abilities (strong vs. weak) and Species Contributions to Beta Diversity (SCBD; high vs. low) for spiders, ants, and beetles. Asterisks indicate significant associations between categories, tested via Chi-square tests (see text for details).

of their conservation value—based only on the contributions made by the wet phase—largely explains this situation, and should be corrected as evidence on the importance of the dry phase emerges. Ongoing climate change and human water overuse is causing significant decreases in streamflow in many rivers (Sabo, 2014; Dettinger et al., 2015), and intermittency is poised to increase in spatial and temporal extent globally in the coming decades (Döll and Schmied, 2012). Thus, the role of dry riverbeds should become central to riverine and riparian conservation.

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Declaration of competing interest The authors declare no conflicts of interest that would inappropriately influence any aspect of the work carried out. Acknowledgments This study was partially funded by the CLITEMP Project (330466; MC-IEF; FP7-people-2012-IEF) and the Seneca Foundation (Project 20645/JLI/18). M.M. Sánchez-Montoya was financially supported by a Marie-Curie postdoctoral fellowship (European Commission), a PIT2 contract at the University of Murcia and the Jiménez de la Espada Programme (20140/EE/17) from the Seneca Foundation. We thank Associate Editor Dr. Liba Pejchar and four anonymous reviewers for their helpful comments, which improved the clarity and quality of the paper. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.biocon.2019.108328. References Acuña, V., Datry, T., Marshall, J., Barcelo, D., Dahm, C.N., Ginebreda, A., McGregor, G., Sabater, S., Tockner, K., Palmer, M.A., 2014. Why should we care about temporary waterways? Science 343, 1080–1081. Acuña, V., Hunter, M., Ruhí, A., 2017. Managing temporary streams and rivers as unique rather than second-class ecosystems. Biol. Conserv. 211, 12–19. Adis, J., Junk, W.J., 2002. Terrestrial invertebrates inhabiting lowland river floodplains of Central Amazonia and Central Europe: a review. Freshw. Biol. 47, 711–731. Allen, D., McCluney, C.K.E., Elser, S.R., Sabo, J.L., 2014. Water as a trophic currency in dryland food webs. Front. Ecol. Environ. 12, 156–160. Baselga, A., 2010. Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19, 134–143. Biswas, S.R., Mallik, A.U., 2010. Disturbance effects on species diversity and functional

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