Occupied and Abandoned Structures from Ecosystem Engineering Differentially Facilitate Stream Community Colonization 1, 1 1 BENJAMIN B

Home , Ecosystem engineer

Occupied and abandoned structures from ecosystem engineering differentially facilitate stream community colonization 1, 1 1 BENJAMIN B. TUMOLO , LINDSEY K. ALBERTSON, WYATT F. CROSS, 2 3 MELINDA D. DANIELS, AND LEONARD S. SKLAR

1Department of Ecology, Montana State University, P.O. Box 173460, Bozeman, Montana 59717 USA 2Stroud Water Research Center, 970 Spencer Road, Avondale, Pennsylvania 19311 USA 3Department of Geography, Planning and Environment, Concordia University, 1455 De Maisonneuve Boulevard West, Montreal, Quebec, Canada

Citation: Tumolo, B. B., L. K. Albertson, W. F. Cross, M. D. Daniels, and L. S. Sklar. 2019. Occupied and abandoned structures from ecosystem engineering differentially facilitate stream community colonization. Ecosphere 10(5):e02734. 10.1002/ecs2.2734

Abstract. Ecosystem engineers transform habitats in ways that facilitate a diversity of species; however, few investigations have isolated short-term effects of engineers from the longer-term legacy effects of their engineered structures. We investigated how initial presence of net-spinning caddisflies (Hydropsychidae) and their structures that provide and modify habitat differentially influence benthic community colonization in a headwater stream by conducting an in situ experiment that included three treatments: (1) initial engineering organism with its habitat modification structure occupied (hereafter caddisfly); (2) initial habitat modification structure alone (hereafter silk); and (3) a control with the initial absence of both engineer and habitat modification structure (hereafter control). Total invertebrate colonization density and biomass was higher in caddisfly and silk treatments compared to controls (~25% and 35%, respectively). However, finer-scale patterns of taxonomy revealed that density for one of the taxa, Chironomidae, was ~19% higher in caddisfly compared to silk treatments. Additionally, conspecific biomass was higher by an average of 50% in silk treatments compared to controls; however, no differences in Hydropsyche sp. biomass were detected between caddisfly treatments and controls, indicating initially abandoned silk structures elevated conspecific biomass. These findings suggest that the positive effects of the habitat modification structures that were occupied for the entirety of the experiment may outweigh any potential negative impacts from the engineer, which is known to be territorial. Importantly, these results reveal that the initial presence of the engineer itself may be important in maintaining the ecological significance of habitat modifications. Furthermore, the habitat modifications that were initially abandoned (silk) had similar positive effects on conspecific biomass compared to caddisfly treatments, suggesting legacy effects of these engineering structures may have pertinent intraspecific feedbacks of the same magnitude to that of occupied habitat modifications. Elucidating how engineers and their habitat modifications differentially facilitate organisms will allow for a clearer mechanistic understanding of the extent to which animal engineers and their actions influence aspects of community organization such as colonization.

Key words: aquatic invertebrates; community recovery; Hydropsyche; legacy effects; silk-producing insects.

Received 30 October 2018; revised 1 March 2019; accepted 26 March 2019. Corresponding Editor: Andrew M. Kramer. Copyright: © 2019 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: [email protected]

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INTRODUCTION potentially positive effects of the additional or altered habitat. Although an engineer and its Facilitation is an important process that influ- modified habitat could be largely conjunct, iso- ences broadscale patterns of community organi- lating the effects of the modification is pertinent zation (Bertness and Leonard 1997, Callaway to our broader understanding of the spatiotem- et al. 2002, Bruno et al. 2003). For example, poral dynamics of ecosystem engineering and plants in terrestrial habitats (Callaway et al. could provide novel insight into ecosystem engi- 2002), along with seaweeds and algae in marine neering consequences (Prugh and Brashares environments (Bertness and Leonard 1997, 2012). Recent research suggests that structural Bracken et al. 2007), can shape spatial patterns of legacy effects of ecosystem engineered facilita- biodiversity through amelioration of harsh phys- tion may be stronger (e.g., void of negative biotic ical environments (e.g., temperature and mois- interactions from the engineer) and occur over ture) and by acting as refugia from negative longer timescales than previously predicted biotic interactions (e.g., grazing and predation). (Jones et al. 1994, Hastings et al. 2007, Sanders Often, facilitation results from ecosystem engi- et al. 2014). For example, negative behavioral neering activities, in which organisms maintain, (e.g., antagonism) and trophic effects (e.g., preda- modify, or create physical habitats that support tion) of an engineer may last a matter of seconds, beneficial conditions for other species (Jones while the engineering structure may persist and et al. 1994, Romero et al. 2015). Ecosystem engi- have effects beyond the life of the engineer (Jones neered habitat modifications, along with the et al. 1994, Hastings et al. 2007, Sanders et al. associated effects on ecological and geomorphic 2014). Elucidating the behavioral and structural processes, are ubiquitous in nature and occur at effects of ecosystem engineers, and how those a variety of scales (Wright and Jones 2006, may vary concurrently over space and time, will Sanders et al. 2014). Furthermore, engineered aid in better understanding and predicting the habitats have been shown to endure severe dis- scales over which ecosystem engineers are most turbance events and persist far beyond the life of relevant. the engineer, leading to legacy effects on Although ecosystem engineering occurs across community dynamics and ecosystem processes nearly all habitats (Jones et al. 1994), the positive (Olafsson and Paterson 2004, Hastings et al. effects on communities are predicted to be great- 2007). Although ecosystem engineers are recog- est in harsh environments, for example, see sup- nized as important facilitators that influence port for the stress gradient hypothesis (Bertness community structure (Hastings et al. 2007, and Callaway 1994, Crain and Bertness 2006, He Albertson and Allen 2015, Romero et al. 2015), and Bertness 2014). Stream ecosystems are we still have limited understanding of the scales uniquely dominated by physical disturbance over which communities are differentially events (Resh et al. 1988) and considered among affected by engineers or their habitat modifica- the most susceptible environments to global tions (Hastings et al. 2007). change with increasingly altered hydrological Despite the potentially wide-reaching conse- regimes, species invasions, and frequent temper- quences of ecosystem engineering, many facets ature extremes (Carpenter et al. 1992, Dodds of habitat engineering animals remain poorly et al. 2004, Tumolo and Flinn 2017). Given these understood (Allen et al. 2014). For example, the environmental gradients and stressors, streams majority of inference surrounding community are fruitful model systems that can be used to effects of animal ecosystem engineers is limited better understand general patterns of ecosystem because investigations typically consider the engineered facilitation (Holomuzki et al. 2010). It combined effects of the engineer and its modifi- has been proposed that the strength of animal cation. This approach, albeit practical, ignores ecosystem engineering within streams is depen- confounding, potentially negative interactions dent on animal body size, density, and behavior between the engineer itself and the community within an abiotic context such as variation in (Gribben et al. 2009). For example, behavioral hydrology associated with seasonal change in attributes of the engineer (e.g., territoriality, flow (Moore 2006). Recently, these hypotheses Gribben et al. 2009) may offset or weaken the were tested in a meta-analysis (Albertson and

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Allen 2015), which revealed that larger animals Cardinale et al. 2004, but see Hemphill and (e.g., migratory salmon) have greater influences Cooper 1983). The nets also have the potential to on physical transport processes than smaller ani- show legacy effects following emergence, death, mals (e.g., insects). However, engineer traits such or downstream drift of the caddisfly itself as biomass were highlighted as particularly (Albertson and Daniels 2016). For example, aban- important because stream insects affected sedi- doned retreats have been shown to persist for ment transport as much as 550 times more than timescales relevant to aquatic insect colonization the larger engineers when accounting for per (i.e., weeks) and withstand extended periods of capita biomass (Albertson and Allen 2015). drought and sediment pollution (Albertson and Behavioral mechanisms in stream ecosystem Daniels 2016). Concurrently, caddisflies have engineering have suggested that interference been shown to be highly territorial and antago- competition is outweighed by facilitation, result- nistic toward animals surrounding their retreats ing in accelerated community recovery following (Hemphill and Cooper 1983, Hemphill 1988). disturbances in empirical studies (Cardinale Thus, untangling facilitation from negative engi- et al. 2001, Hammock and Bogan 2014). Addi- neer traits (e.g., interference competition) has tionally, resilience of ecosystem engineered struc- particular relevance in understanding how this tures in lotic environments (e.g., beaver dams) engineer and its habitat modification influence has been shown to have strong legacy effects on community assembly following disturbance ecosystem function and persist for several gener- events (Cardinale et al. 2001). Collectively, these ations after the death of the engineer (Hastings aspects of net-spinning caddisfly ecology pro- et al. 2007). Progress has been made in investi- vide an ideal system to dissect the positive and gating the intricacies of engineering effects negative effects of the engineer vs. the engi- within terrestrial, marine intertidal, and lake sys- neered structure on stream communities over tems (Callaway et al. 2002, Olafsson and time. Paterson 2004, Wright and Gribben 2017); how- We tested whether the initial presence of cad- ever, we have only begun to understand their disflies and/or caddisfly silk influences character- importance within stream ecosystems. istics of invertebrate colonization within a Here, we examine engineering effects of net- headwater stream. Specifically, we tested spinning caddisfly-mediated facilitation on invertebrate communities in a headwater stream. Net-spinning caddisflies (Trichoptera:Hydropsy- chidae) are aquatic insect larvae that act as ecosystem engineers within headwater streams by modifying the environment in several ways (Fig. 1). These animals build silk catch-nets with retreats of organic/inorganic material among streambed substrate that allow them to passively feed on items flowing through the water column. The silk nets and retreats locally ameliorate habitat by markedly decreasing local hydraulic velocity (Juras et al. 2018), thereby creating stream bed heterogeneity (Diamond 1986, Cardinale et al. 2002) and micro-flow refugia for certain taxa (Nakano et al. 2005). The silk can also act as a stabilizer of gravels and altering sediment disturbance during flood events (Statzner et al. 1999, Cardinale et al. 2004, Johnson et al. 2009, Albertson et al. 2014). Furthermore, caddisfly engineering is highly relevant to colonization Fig. 1. A caddisfly with its retreat and silk net struc- dynamics following disturbance events because ture holding stream gravels together. Photo credit: net-spinners are early colonizers (Hemphill 1988, Benjamin B. Tumolo.

❖ www.esajournals.org 3 May 2019 ❖ Volume 10(5) ❖ Article e02734 TUMOLO ET AL. whether the initial presence of caddisflies and 1982). Second, this timescale is particularly rele- their silk (hereafter caddisfly, a treatment that vant to the duration over which caddisfly silk included both engineer and habitat modification material is known to last without the engineer structure) influenced macroinvertebrate colo- itself present (Appendix S1: Fig. S1; Albertson nization differently than the initial presence of and Daniels 2016). The East Branch of WCC is caddisfly silk alone (hereafter silk, a treatment classified as a third-order piedmont stream with that included just the habitat modification struc- land use predominated by forest and agriculture ture) or controls with initial absence of (Newbold et al. 1997). In our study location, caddisflies and silk (hereafter control). These median bed material grain size is approximately treatments, respectively, represent (1) the pres- 35 mm, riffle width is 5 m, and shade cover is ence of caddisflies prior to colonization of other 50% (Albertson et al. 2018). Our experiment was invertebrates, including conspecifics, because initiated with three treatments: initial caddisflies they are early colonists (Cardinale et al. 2004), (2) present with their silk structures (caddisfly), ini- caddisfly structures alone persisting through a tial habitat modification structure of caddisfly disturbance event (Albertson and Daniels 2016), silk alone (silk), and a control treatment with ini- (3) and a post-disturbance scenario without early tially no caddisflies or silk present (control). The caddisfly colonization or legacy of the silk. We silk treatment allowed us to test whether initial predicted that (1) the initial presence of caddis- removal of engineer traits (e.g., territorial behav- flies with silk and silk alone would increase iors or structural maintenance) when caddisflies invertebrate colonization rate and overall benthic are absent influences the role of the habitat modi- density and biomass compared to controls, (2) fication structure itself on the trajectory of overall the initial presence of caddisfly silk alone would colonization patterns. This technique has been increase invertebrate colonization rate, and over- used to isolate the effects of aquatic silk engineer- all benthic density and biomass, compared to a ing structures in a previous study (Hammock treatment with caddisflies initially present due to and Bogan 2014). Treatments were initiated for the potential negative effects (e.g., territorial measurement of in situ invertebrate colonization interactions) of the caddisflies offsetting the posi- in flow-through plastic mesocosms (0.90 m tive effects of silk structures, and (3) the impor- long 9 0.124 m wide 9 0.135 m deep) with 20- tance of initial silk or caddisfly presence would mm plastic mesh secured to the upstream and vary throughout the temporal duration of the downstream ends (Appendix S1: Fig. S2). Meso- experiment, if treatments converged over time cosms were designed to keep gravels within the when Hydropsychidae naturally colonized all experimental units while allowing for natural treatments. Our findings provide insight into the water flow and invertebrate colonization. Meso- complex ecological dynamics that control how cosms were carefully filled by hand with a sub- ecosystem engineers may facilitate habitat for surface layer of pea gravel (~5–10 mm) and then other organisms and the relative importance of covered with a surface layer 1 grain diameter engineering structures vs. engineer interactions. thick (median grain size of 45 mm). Surface layer gravels were quarried from WCC, while subsur- METHODS face gravels were purchased. All experimental gravels were dry and denuded of biofilm prior to Experimental design the experiment for >6 months. The mesocosm We conducted our study in the headwaters of habitat was designed to represent an armored the East Branch of White Clay Creek (hereafter surface layer typical of a recently disturbed WCC, 39°51059.3″ N75°47009.4″ W) located in (denuded of biofilm) gravel-bedded river Avondale, Pennsylvania, from 25 May 2016 to 30 (Dietrich et al. 1989). June 2016. The duration of the experiment (30 d) To create the experimental treatments, hydropsy- was chosen to represent aspects of the study sys- chid caddisflies (Hydropsyche spp.) of the same tem’s flashy disturbance regimes and organismal developmental stage (3rd–4th instar) were hand life histories. First, macroinvertebrates in streams collected from WCC over a 24-h period (average are known to rapidly recolonize disturbed areas length = 13.9 0.11 mm, average dry weight = within a matter of days to weeks (Fisher et al. 5.29 0.25 mg; n = 15 reference samples). Each

❖ www.esajournals.org 4 May 2019 ❖ Volume 10(5) ❖ Article e02734 TUMOLO ET AL. mesocosm of the caddisfly and silk treatments established, individual mesocosms were care- was inoculated with 134 caddisflies, equivalent fully moved and placed into WCC. One meso- to a density of 1, 290 m 2. Caddisfly densities of cosm of each treatment was placed in each of these magnitudes are widely reported through- eight consecutive riffle habitats within WCC for out the eastern United States and are conserva- a total of n = 8 for each treatment. We selected tive for WCC, which can host over 10,000 mesocosm site locations with similar physical rif- hydropsychids/m2 (Cardinale et al. 2004, Albert- fle conditions (water depth, channel width, ripar- son et al. 2018). Caddisfly inoculation was con- ian vegetation) and randomized treatment ducted in stream-side flume channels (Appendix position at each site to ensure a treatment was S1: Fig. S2), and caddisflies were given 48 h to not confounded by its proximity to the left or build silk nets (Albertson et al. 2014). Control right stream banks. Mesocosms were secured mesocosms were also placed in neighboring but with rebar and recessed within surrounding sub- isolated stream-side flumes; however, no caddis- strates. During the experiment, detritus was flies were added. Flumes were kept wet during removed from the upstream end of mesocosms treatment initiation by pumping water from every 24 h. WCC through a series of settling tanks and We did not maintain experimental treatments screens, which prohibited the transport of throughout the duration of the experiment by macroinvertebrates into experimental meso- continually removing Hydropsyche spp. individu- cosms during initiation (Appendix S1: Fig. S2). als from control and silk treatments. Instead, all Following the 48-h colonization period, individ- treatments were equally exposed to natural colo- ual caddisflies from the silk treatment were nization of Hydropsyche spp. once moved into removed from nets and gravels within the meso- WCC (see Results) with potential for treatment cosm with forceps while leaving silk material convergence over time. This design allowed us to intact, a method successfully used with other address our goal of testing the effects of initial aquatic silk-producing insects (Hammock and experimental treatments on total invertebrate col- Bogan 2014). Some caddisflies crawled below the onization, including other hydropsychids. We surface gravels; thus, to ensure the desired treat- chose this approach allowing for potential con- ment was accomplished, each piece of surface vergence of treatments over time for three pri- gravel was lifted and the subsurface layer was mary reasons. First, our experiment aimed to inspected. While we recognize that this tech- measure the effect of initial presence of engineers nique potentially broke or stretched silk strands or their habitat modification structures given the connecting adjacent gravels, thereby reducing recognized importance of colonization history in one mechanism for invertebrate facilitation shaping community assemblage (Cardinale et al. related to gravel stabilization, our study was con- 2001). Second, it would be logistically challeng- ducted at baseflow when gravels were not mobi- ing to exclude Hydropsyche spp. colonists without lized by high flows. Perhaps most importantly, confounding the colonization of other taxa, this technique did not interrupt the presence of which would further constrain the ecological rel- silk on rock surfaces (i.e., not between gravels), evance of the experimental design. Third, where it reduces flow velocity and acts as an hydropsychids are an abundant member of head- important facilitation pathway for benthic inver- water stream communities (Cardinale et al. 2001, tebrate taxa seeking flow refuge and optimized 2004, Albertson et al. 2014), and being able to food delivery (Cardinale et al. 2002, Nakano evaluate potential positive and/or negative feed- et al. 2005). Following manipulation, individual backs between the initial presence of this particu- mesocosms were promptly returned to the artifi- lar taxon and the final presence of this same cial channel. The caddisfly and control treatment taxon is ultimately important to advance under- gravels were treated identically to the silk treat- standing of these headwater stream ecosystems. ment (i.e., surface gravels were briefly lifted); however, caddisflies were not removed from the Sampling and processing of invertebrate caddisfly treatment and no caddisflies were colonization present in the control. After all of the meso- Invertebrates were sampled from individual cosms were manipulated and treatments were mesocosms once every 24 h for the first five days

❖ www.esajournals.org 5 May 2019 ❖ Volume 10(5) ❖ Article e02734 TUMOLO ET AL. of the experiment and then once every five days dominant taxa biomass, and richness across for the next 25 d for a total of 10 sampling treatments included the fixed effects of treatment events. During each sampling event, three ran- and day and random effects of site alone and domly selected surface gravels were removed individual mesocosm (Tank) nested within site, and placed on a 150-lm sieve. Rocks were nested within sampling date as represented here: sprayed with filtered water over the sieve and lmerðResponse Treatment Day visually inspected to ensure all macroinvertebrates were removed. Rocks were then towel- þð1jSite=TankÞ; data ¼ databasenameÞ dried and marked with a permanent marker (to These models accounted for the non-indepen- avoid resampling) and placed back in the meso- dence of samples taken at the same mesocosm cosm. Invertebrates collected in the sieve were over multiple sampling events by using a stan- transferred to a Whirl-Pak, preserved with 70% dard mixed-model repeated-measures design ethanol and transported to the laboratory. where mesocosm was nested within sampling Invertebrates were enumerated, measured in date (Bolker 2008, Zuur et al. 2009). Coloniza- length to the nearest mm, and identified to genus tion rate was calculated by fitting a linear or lowest practical taxonomic level (Merritt and regression to the number of invertebrates per Cummins 1996, Smith 2001). Total invertebrate sample colonized over the first 10 d of the biomass in each sample was estimated as mg ash experiment. Colonization rate was analyzed free dry mass (AFDM) per sample using estab- with a fixed effect of treatment and a random lished taxon-specificlength–mass relationships effect of site because distinction of sampling (Benke et al. 1999). Invertebrate taxon richness date was precluded as this metric subsumed val- was estimated as the total number of unique taxa ues from the first 10 d of the experiment. Inver- per sample. All surface gravels used in the experi- tebrate density and biomass were calculated for ment were photographed, and surface area was the three dominant taxa. Density and biomass of measured to the nearest mm with ImageJ the total community, as well as dominant taxa, (National Institutes of Health, Bethesda, Mary- were natural log-transformed to meet assump- land, USA). Preliminary analyses showed no sig- tions of normality. All mixed-effects models nificant differences in rock size among treatments; were fit with the lme4 package (Bates et al. therefore, density was estimated as no. per sam- 2014), and significance was tested using a Ken- ple and overall biomass as mg AFDM per sample. ward-Roger denominator degrees of freedom For the caddisfly treatments, all Hydropsyche spp. approximation (Kenward and Roger 1997, ≥13 mm length (i.e., the individuals initially Bolker et al. 2009). Post hoc comparisons of least added to the caddisfly treatment mesocosms) was squares means and confidence intervals for removed from further analyses to avoid con- response variables between treatments were cal- founding our initial caddisfly inoculation with culated using the lsmeans function (Lenth and natural colonization of other taxa and/or newly Herve 2015). All linear mixed-effects model colonizing individuals of this taxon. Additionally, analyses were conducted using R version 3.3.1 preliminary analyses showed that three taxa (Chi- (R Development Core Team 2016). ronomidae, Hydropsyche spp. and Baetis spp.) con- Invertebrate community composition was tributed to over 80% of the overall invertebrate compared among treatments using non-metric density; thus, additional analyses considered the multi-dimensional scaling (NMDS) applied to a density and biomass between treatments of each Bray–Curtis dissimilarity matrix based on of these dominant taxa separately. square-root-transformed density to account for weighted contribution of rare and common taxa Data analysis (Zar 1996). Non-metric multi-dimensional scal- Total invertebrate density and biomass, the ing on a Bray–Curtis dissimilarly matrix is dominant taxa’s density and biomass, species widely practiced in community ecology as it pro- richness and colonization rate were analyzed vides robust inference to unconstrained ordina- using linear mixed-effects models. Linear mixed- tion of ecological variables in multivariate space effects models comparing invertebrate density, (Kruskal 1964, Faith et al. 1987, McCune et al. invertebrate biomass, dominant taxa density, 2002). The NMDS ordination was conducted

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= = using PRIMER-E v.6.2 (PRIMER-E Ltd, Ivy- sample, t14 2.27, P 0.040). Silk treatments bridge, UK; Clarke and Gorley 2006) with several showed an increase in total density after day 15 fi = = random starting con gurations; the lowest stress of the experiment (F9, 189 14.26, P 0.001; was selected after 20 trials for a 2-dimensional Fig. 2a, Table 1; Appendix S1: Table S1). These solution. To test for differences in invertebrate temporal differences in total density of the silk communities among treatments, we conducted treatment can be attributed to patterns of higher an analysis of similarity (ANOSIM) using the Chironomidae density observed after day 15 – = = Bray Curtis distance matrix with 999 permuta- (F9, 189 13.93, P 0.001, Fig. 3c, Table 1; tions (Oksanen et al. 2007). Taxa influencing Appendix S1: Table S2). In addition, initial cad- community structure of treatments were identi- disfly presence had a consistent positive effect by fied using a similarity percentage analysis (SIM- increasing Chironomidae density compared to PER). Field experiments are expected to have control and silk treatments throughout the dura- high variability among sampling replicates; tion of the experiment, but especially up to day fi = = therefore, all analyses were tested for signi cance 15 (F2,14 7.30, P 0.07; Fig. 3c, Table 1; at alpha a = 0.05 and marginal significance at Appendix S1: Tables S1, S2). Overall Chironomi- a = 0.1. Finally, because our goal was to directly dae density was 37% higher in caddisfly compare how caddisflies and their silk habitat treatments compared to controls (64.69 7.47 modification structures influence invertebrate vs. 40.68 7.48 Chironomidae per sample, = = communities, our analysis only considered inver- t14 3.82, P 0.002) and 19% higher compared tebrates within the experimental mesocosms, to silk (64.69 7.47 vs. 52.28 7.48 Chironomi- = = and we did not compare how our experimental dae per sample, t14 1.98, P 0.068). Further- treatments related to ambient unmanipulated more, Chironomidae density was 29% higher in invertebrate characteristics of WCC. silk compared to control treatments with mar- fi = = ginal statistical signi cance (t14 0.20, P RESULTS 0.086). No treatment effects were detected for density of Hydropsyche spp. and Baetis spp. Throughout the experiment, a total of 20,576 (P > 0.15, Table 1; Appendix S1: Table S1). invertebrates of 54 unique taxa were collected We detected a significant difference in biomass fi = = and identi ed from mesocosms. The three among treatments (F2,14 4.68, P 0.023; dominant taxa collected during the experiment Fig. 2b; Appendix S1: Table S1), with a 35% were Chironomidae, which comprised 61.3%, increase of overall biomass in caddisfly com- Hydropsyche spp., which accounted for 16.4%, pared to control treatments (3.39 0.66 vs. fl = and the may y genus, Baetis spp., which com- 2.19 0.66 mg AFDM per sample, t14 2.56, prised 6.7% of total individuals. P = 0.049), and silk treatments had 45% higher Invertebrate density showed patterns of rapid overall biomass compared controls (4.01 0.66 = colonization across treatments, with consistently vs. 2.19 0.66 mg AFDM per sample, t14 2.56, higher values recorded in caddisfly and silk P = 0.003); however, there were no differences in = fl treatments compared to controls (F2,14 4.98, overall biomass between silk and caddis y treat- P = 0.021; Fig. 2a, Table 1; Appendix S1: Tables ments (P = 0.3, Table 1; Appendix S1: Table S1). S1, S2). These patterns were most evident When split up by the dominant three taxa initial through day 15 of the experiment, after which caddisfly presence had positive effects on = time invertebrate density began to converge Chironomidae biomass relative to controls (F2,14 among all treatments (Fig. 2a). Overall inverte- 7.42, P = 0.006; Fig. 3f, Table 1; Appendix S1: brate density was 31% higher in caddisfly treat- Tables S1, S2), increasing chironomid biomass by ments than in control (83.31 10.89 vs. 45% (0.76 0.11 vs. 0.42 0.11 Chironomidae = = = 57.21 10.90, individuals per sample, t14 3.09, mg AFDM per sample, t14 3.83.56, P 0.002) P = 0.008); however, no differences were found and initial silk presence increased chironomid bio- between caddisfly treatments and silk (P = mass by 32% compared to controls (0.63 0.11 vs. 0.423). Overall invertebrate density was 25% 0.43 0.11 Chironomidae mg AFDM per sample, = = higher in silk treatments than in controls t14 2.24, P 0.04). However, no differences in (76.34 10.89 vs. 57.21 10.90 individuals per Chironomidae biomass were detected between

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Fig. 2. Experimentally measured mean values ( standard error) with line loess ﬁt of (a) invertebrate density (individuals per sample) and (b) invertebrate biomass (mg AFMD per sample) compared between caddisﬂy, silk, and control treatments samples across the ten sampling dates of the experiment.

Table 1. Summary table of treatment effects on overall invertebrate density, biomass, colonization rate, and differences in dominant invertebrate density and biomass of Hydropsyche sp., Baetis sp., and Chironomidae compared between caddisﬂy, silk, and control treatments across the ten sampling dates of the experiment.

Outcome Metric Caddis vs. Control Silk vs. Control Caddis vs. Silk

Overall density Caddis > Control 31% Silk > Control 25% No difference Overall biomass Caddis > Control 35% Silk > Control 45% No difference Richness No difference No difference No difference Colonization rate No difference No difference No difference Chironomidae density Caddis > Control 45% Silk > Control 32% Caddis > Silk 19% Baetis density No difference No difference No difference Hydropsyche density No difference No difference No difference Chironomidae biomass Caddis > Control 45% Silk > Control 32% No difference Baetis biomass No difference No difference No difference Hydropsyche biomass No difference Silk > Control 50% No difference

fl = = fl = silk and caddis y treatments (t14 1.60, P or caddis y and control treatments (P 0.2). The 0.133, Table 1; Appendix S1: Tables S1, S2). Fur- result of greater Hydropsyche biomass and lower thermore, initial presence of silk increased density in the silk treatment compared to the Hydropsyche spp. biomass by 50% relative to caddisfly treatment demonstrates that the same controls (Fig. 3d, 2.87 0.55 vs. 1.43 0.55 densities of larger sized individual Hydropsyche = Hydropsyche mg AFDM per sample, t14 2.74, P spp. colonized silk treatments compared to con- = 0.011); however, no differences were detected trol and caddisfly treatments (Fig. 3a vs. d). Pat- between silk and caddisfly treatments (P = 0.2) terns in Baetis spp. biomass did not show any

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Fig. 3. Experimentally measured mean values ( standard error) with line loess fit of dominant invertebrate density (individuals per sample) and biomass (mg AFDM per sample) of Hydropsyche sp. (a, d), Baetis sp. (b, e), and Chironomidae (c, f), compared between caddisfly, silk, and control treatments across the 10 sampling dates of the experiment. differences among treatments throughout the locations of communities, further suggesting = duration of the experiment (F2,14 1.67, similar general composition among treatments. P = 0.222; Fig. 3e, Table 1; Appendix S1: Table S1). DISCUSSION No differences were detected in richness (P = 0.78) or colonization rate (calculated as Facilitation by habitat amelioration can influ- number of invertebratessample 1d 1) over the ence community structure and recovery, and pos- first ten days of the experiment (P = 0.26) among itive interactions are increasingly recognized as a treatments, suggesting there were no differences fundamental driver of ecological organization in invertebrate community composition among comparable in strength to that of predation and initial treatments throughout the experiment competition. Furthermore, facilitation by habitat (Table 1; Appendix S1: Table S3). Additionally, transformation has been documented across ter- overall invertebrate community composition restrial, marine and freshwater environmental pooled across time showed high overlap among gradients where ecosystem engineers may serve treatments based on NMDS and ANOSIM analy- as important targets for conservation (Crain and ses (Appendix S1: Fig. S3, 2D stress = 0.15, Bertness 2006, Romero et al. 2015). Few studies, ANOSIM Global R = 0.002, P > 0.9) suggested however, have evaluated the different effects of no overall community differences among treat- engineers and their habitat modification struc- ments. The SIMPER analysis indicated 18 taxa tures or have considered the legacy effects of contributed to ~90% of the multivariate locations such habitat transformations on community of communities in initial caddisfly, silk and con- dynamics following the loss of the engineer. Our trol treatments. In all treatment comparisons, study shows that (1) the initial presence of an Chironomidae, Hydropsyche spp., Baetis spp., and ecosystem engineer (Hydropsyche spp.) and its Simuliidae explained ~52% of multivariate abandoned structure increased aspects of

❖ www.esajournals.org 9 May 2019 ❖ Volume 10(5) ❖ Article e02734 TUMOLO ET AL. invertebrate colonization, (2) the initial presence providing food supplements. For example, of the engineer had variable effects on certain Nakano et al. (2005) showed that caddisfly taxa compared to initially abandoned engineer- retreats provide low-flow refugia and increase ing structures, (3) positive effects of the engineer abundances of mayflies (Ephemerella). Our analy- and their structure outweighed presumed nega- sis showed that densities of Chironomidae, a tive engineer traits, and (4) initially abandoned family of aquatic insects with even lower flow engineered structures positively affected con- preferences compared to those of Ephemerella specific biomass similarly to initially occupied (Armanini et al. 2011), were greater in the pres- structures, suggesting that positive legacy effects ence of caddisflies and silk indicating flow refuge of engineering structures occur at similar magni- as a possible mechanism for habitat facilitation in tudes to occupied engineering structures. our study system. Indeed, these experimental findings and hypotheses are supported by Facilitation by caddisflies hydraulic modeling demonstrating up to a 60% Our analysis showed that the initial presence reduction of interstitial flow velocity in the pres- of caddisflies and silk facilitated patterns of local ence of caddisfly silk structures (Juras et al. invertebrate density and biomass differently dur- 2018). Caddisflies also stabilize surface gravels ing colonization. These findings were partly con- and decrease sediment disturbance by increasing sistent with our prediction that caddisflies would critical bed shear stress (Cardinale et al. 2004, facilitate invertebrate colonization density and Albertson et al. 2014), which may further biomass, namely by supporting chironomids and improve physical habitats for invertebrates by hydropsychids. However, our findings differed providing a refuge from scour (Brittain and Eike- from our predictions in that abandoned ecosys- land 1988). Along with the physical habitat ame- tem engineering structures only had greater posi- lioration, the silk of caddisflies and other stream tive effects than caddisfly presence in terms of insects (Diptera:Simuliidae) has also been shown conspecific biomass. Patterns of local aquatic to transfer water column food resources to the invertebrate density and biomass could have streambed, possibly increasing food availability implications for ecosystem function, as this to secondary producers such as invertebrates group of organisms represents an important food (O’Connor 1993, Hammock and Bogan 2014). web linkage between basal resources and higher Thus, we hypothesize that caddisflies facilitate trophic levels within and across ecosystem invertebrate colonization through a combination boundaries (Baxter et al. 2005). However, the rel- of non-mutually exclusive mechanisms of physi- evance of our results to these broader scale pre- cal habitat amelioration and increased food avail- dictions needs to be tested in future experiments ability, which may have consequences ranging and under natural field conditions. Perhaps from the population to community level. These unsurprisingly, the majority of research regard- mechanisms remain to be tested and should be ing animal engineering across a variety of ecosys- considered in future experiments. tems has focused on the impact of large bodied We predicted that caddisflies and their silk vertebrates, such as beavers and their extensive would influence other characteristics of commu- dam complexes (Naiman et al. 1988, Hastings nities, such as colonization rate and composition; et al. 2007) or elephants and bison clearing vege- however, we found no such patterns. These find- tation (Haynes 2012). In this study, we echo a ings suggest that the initial presence of caddis- growing body of work demonstrating large flies and silk did not influence the speed or effects of small invertebrates (<1 cm) on local composition of community assembly within a community characteristics, highlighting the sig- headwater stream. The underlying mechanisms, nificance of numerically abundant, small-bodied food availability or flow disturbance refuge, for ecosystem engineers (Olafsson and Paterson caddisfly facilitation were not tested, making it 2004, Benelli et al. 2018). difficult to evaluate why there were changes Previous studies have shown that caddisfly measured in density and biomass and not in engineering increases abundances of certain composition. However, other studies have invertebrates at local scales, perhaps by reducing shown similar patterns of habitat modification flow velocity, increasing heterogeneity, or resulting in changes in abundance with little

❖ www.esajournals.org 10 May 2019 ❖ Volume 10(5) ❖ Article e02734 TUMOLO ET AL. effect on community structure. For example, communities, with particular attention to the extensive habitat modification by grazing of effects of land use, invasive species, and ecosystem migratory fishes has been shown to drastically engineering (Cuddington 2011, Ruffing et al. alter invertebrate abundance with variable, less 2015). Our study presents evidence that experi- predictable patterns of community structure mentally abandoned engineered structures can response (Flecker 1996). Perhaps our analysis influence colonization of community density, bio- shows that engineered habitat can result in more, mass, and conspecifics in a headwater stream for yet functionally equivalent habitat (i.e., caddisfly at least 30 d (Fig. 2; Appendix S1: Figs. S1, S3), retreats may provide habitat similar to that of suggesting that caddisfly structures may persist important interstitial pore spaces within the and continue to have positive legacy effects. Cad- gravel bed), leading to greater abundances but disflies frequently drift downstream from their not changes in community composition. retreats as a means of dispersal (Brittain and Eike- Contrary to our predictions, we found initial land 1988, Benke et al. 1991) and predator avoid- presence of caddisflies had similar effects on den- ance (Fairchild and Holomuzki 2005). If caddisfly sity and biomass compared to silk treatments; nets remain intact during and after a drift-indu- however, important aspects of overall density cing disturbance, based on our results, community and biomass were influenced differently by cad- density, biomass, and conspecificbiomassshould disfly and silk presence. Specifically, we show experience legacy effects from caddisflyengineer- that initial caddisfly presence increases Chirono- ing. However, other aspects of invertebrate colo- midae density compared to silk treatments, while nization that were affected by initial caddisfly initial silk presence increases body sizes of con- presence (Chironomidae density) were affected specific colonizers compared to initial caddisfly less by initially abandoned ecosystem engineering presence. Our results contrast with earlier work structures. These differences in facilitation suggest showing competitive exclusion of other stream the presence of the engineer with its habitat modi- invertebrates by hydropsychids (Hemphill and fication may be important in maintaining function Cooper 1983, Diamond 1986, Hemphill 1988) of ecosystem engineered structures and conse- and intense fighting between conspecifics (Eng- quently its positive effects on the community. lund and Olsson 1990). However, our results are Indeed, hydropsychids are known to tend their congruent with other patterns observed in cad- nets so as to keep them clear of suspended sedi- disfly and blackfly larvae colonization studies ments and to alter mesh pore spacing in variable (Cardinale et al. 2002, Hammock and Bogan flow conditions (Runde and Hellenthal 2000), and 2014), suggesting competition and behavioral perhaps these maintenance activities are important antagonism of the caddisfly engineer can be neg- in regulating the extent to which caddisflies ligible and/or offset by the positive effects of facilitate Chironomidae colonization. Furthermore, facilitative habitat modification. Furthermore, these differences in engineering effect between findings of conspecific legacy effects on occupied and abandoned habitat modifications Hydropsyche spp. biomass from initially aban- have broad implications for the way communities doned engineering structures align with observa- organized by ecosystem engineers are targeted for tions of larger instar caddisflies taking over conservation and restoration purposes (Byers et al. abandoned retreats (Englund and Olsson 1990). 2006). For example, management strategies Broadly, these results highlight the importance of designed to mimic benefits of naturally occurring untangling simultaneous effects of engineers and ecosystem engineering structures and relation- their habitat modifications and developing a fur- ships, such as beaver dam analogs, may only offer ther understanding of species interaction net- a fraction of ecological services provided by the works and community effects of ecosystem engineer in conjunction with its habitat engineering (Prugh and Brashares 2012). modification (Pollock et al. 2014). Taken together, legacy effects of caddisfly structures were Does what you leave behind count? shown to have a pertinent feedback; however, Recent advances in geomorphology and ecology community effects of ecosystem engineering have recognized the importance of legacy in were greatest with the initial presence of the engi- shaping physical landscapes and biological neer.

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Study limitations abandoned habitat modification structure, sug- Even given the strong evidence we detected gesting engineer presence may be important in for positive effects of initial presence of caddisfly maintaining facilitative habitat modifications. larvae and their silk structures on benthic taxa, Finally, we detected evidence of abandoned our findings should be interpreted with caution. habitat modifications increasing conspecific bio- Because our study was conducted within in situ mass, signifying caddisfly engineers may have mesocosms, the potential for the same patterns to intraspecific legacy effects, manifesting at equal develop at broader reach-scales, where coloniza- magnitudes and temporal scales as the effects of tion and dispersal dynamics occur across larger occupied habitat modifications. Our study shows distances of natural river ecosystems is unknown positive community-level changes resulting from (Brown and Swan 2010). Although we did not ecosystem engineering, highlighting the impor- investigate how the changes to invertebrate den- tance of intricate animal ecologies involved in sity and biomass that we detected might influ- animal–environment relationships. Continued ence ecosystem processes or trophic dynamics, appreciation of these abiotic and biotic feedback we suspect that they could influence resource loops and their respective legacies may further processing or availability for higher trophic levels our understanding of multi-scale community (Gracßa 2001), and future work should measure dynamics (Allen et al. 2014). how and when. Additionally, our experiment only encompassed a limited range of gravel sizes ACKNOWLEDGMENTS and flow conditions, when a broader range of fl fl gravel sizes and ow regimes (e.g., ooding or We thank N. Beckman for his time spent identifying drought) are common in natural streams, and invertebrates and V. Ouellet for field assistance. We these physical factors are highly relevant to colo- also thank J. Junker, E. Scholl, W. Glenny, M. MacDon- nization dynamics of benthic stream inverte- ald, and M. P. Moore for their constructive dialogue brates (Fisher et al. 1982). Finally, we did not and help with analysis. Finally, we are thankful for maintain treatments, so the initial control and ini- two anonymous reviewers whose comments led to a tial silk only treatments converged with the greatly improved manuscript. Funding for this project caddisfly treatments. We believe this conver- was provided by the National Science Foundation (DEB 1556684). The authors declare they have no con- gence reasonably captures colonization dynamics flicts of interest regarding this work. of the entire invertebrate assemblage, including hydropsychids, but also acknowledge that this LITERATURE CITED experimental approach weakens our ability to isolate effects of just silk alone. Despite these Albertson, L. K., and D. C. Allen. 2015. Meta-analysis: limitations, however, our conclusions remain Abundance, behavior, and hydraulic energy shape strongly consistent with our original hypotheses biotic effects on sediment transport in streams. and warrant further exploration. Ecology 96:1329–1339. Albertson, L. K., and M. D. Daniels. 2016. Resilience of CONCLUSION aquatic net spinning caddisfly silk structures to common global stressors. Freshwater Biology Our study shows initial presence of ecosystem 61:670–679. engineering caddisflies, and their structures have Albertson, L. K., V. Ouellet, and M. D. Daniels. 2018. positive effects on local invertebrate density and Impacts of stream riparian buffer land use on fi biomass within a headwater stream ecosystem. water temperature and food availability for sh. – Our results suggest potential negative behavioral Journal of Freshwater Ecology 33:195 210. Albertson, L. K., L. S. Sklar, P. Pontau, M. Dow, and B. (i.e., antagonism) and/or consumptive effects of J. Cardinale. 2014. A mechanistic model linking the caddisfly engineer were offset by positive fi insect (Hydropsychidae) silk nets to incipient sedi- effects (i.e., facilitation) of the habitat modi ca- ment motion in gravel-bedded streams. Journal of fi tion. Additionally, our ndings reveal that posi- Geophysical Research: Earth Surface 119:1833– tive effects on local Chironomidae density 1852. associated with initial engineer presence did not Allen, D. C., B. J. Cardinale, and T. Wynn-Thompson. occur in the initial presence of the engineers’ 2014. Toward a better integration of ecological

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