Journal of Animal Blackwell Publishing Ltd. Ecology 2003 Caddisfly diapause aggregations facilitate benthic 72, 1015–1026 invertebrate colonization
DECLAN J. MCABE and NICHOLAS J. GOTELLI Department of Biology, University of Vermont, Burlington, Vermont, 05405, USA
Summary 1. We used natural and manipulative field experiments to examine the effects of cad- disfly (Trichoptera) diapause aggregations on benthic macroinvertebrates communities in a Vermont river. 2. Natural substrates with aggregations of Neophylax and Brachycentrus (Trichoptera: Uenoidae and Brachycentridae) had higher species richness than did substrates lacking aggregations. Aggregations of caddisfly cases added to artificial substrates (bricks) also accumulated greater abundance, species density (number of species per unit area), and species richness (number of species per standard number of individuals) than did con- trol bricks. 3. Low-density, uniformly spaced, Brachycentrus cases accumulated higher species density and species richness than did an equivalent density of clumped cases. Similarly, empty Neophylax cases accumulated higher diversity than did cases still occupied by Neophylax pupae. 4. Although natural substrates had higher species richness than artificial substrates, substrate type did not change qualitatively the effect of caddisfly aggregations on spe- cies richness. 5. We subsampled individuals randomly from aggregations and control surfaces to provide an estimate of species richness unbiased by abundance. Expected species richness was higher in aggregations than on control surfaces. These results suggest that caddisfly aggregations increase species density by altering the shape of the species–abundance distribution as well as by accumulating individuals and species passively. 6. We conclude that caddisfly diapause aggregations increase habitat complexity and facilitate colonization of other benthic species. Key-words: biogenic structures, community, ecosystem engineering, positive interactions, rarefaction. Journal of Animal Ecology (2003) 72, 1015–1026
actions are important in communities of plants (Andersen Introduction & MacMahon 1985; Chapin et al. 1994; Tardiff & Stanford After decades of neglect (Boucher, James & Keeler 1998; Holzapfel & Mahall 1999), marine invertebrates 1982; Hunter & Aarssen 1988; Bertness & Callaway (Duggins 1981; Gallagher, Jumars & Trueblood 1983; 1994; Stachowicz 2001), the study of positive interac- Wieczorek & Todd 1997; Wieczorek & Todd 1998) and tions in ecological communities has recently enjoyed a freshwater invertebrates (Pringle 1985; Diamond 1986; resurgence of interest (Poulin & Grutter 1996; Hacker Englund & Evander 1999; Stewart et al. 1999). & Gaines 1997; Kareiva & Bertness 1997; Holzapfel & Positive interactions may be pervasive because some Mahall 1999; Cardinale, Palmer & Collins 2002). species act as ‘ecosystem engineers’, creating or modi- Although studies of competition and predation con- fying habitats that are used by other species (Jones, tinue to dominate community ecology, positive inter- Lawton & Shachak 1994). A large-scale example of ecosystem engineering is a beaver dam, which alters Correspondence and present address: Declan J. McCabe, stream flow and sedimentation (Pollock et al. 1995). Department of Biology Box 283, St Michael’s College, 1 On a smaller scale, the shells, cases and tubes of sessile © 2003 British Winooski Park, Colchester, VT 05439, USA. Tel. (802) 654 2626; invertebrate species may stabilize substrates and/or Ecological Society Fax: (802) 654 2236; E-mail: [email protected] increase area and complexity of habitats that are
1016 available to other colonizing species (Gallagher et al. D. J. McCabe & 1983; Pawlik, Butman & Starczak 1991). Organisms N. J. Gotelli that facilitate community-level colonization may also be considered ‘keystone species’ if the magnitude of their influence far exceeds expectations based on their biomass (Power et al. 1996). In this paper, we tested the role of case-bearing cad- disfly larvae as facilitators of colonization in benthic stream assemblages. In streams of North America, larvae of Brachycentrus (Curtis) and Neophylax (McLachlan) form dense aggregations on rock sur- faces, and their cases can persist for weeks (in the instance of Brachycentrus) to months (for Neophylax). In a natural experiment, we measured the species rich- ness and species density of macroinvertebrates on rock surfaces with and without caddisfly cases. In a field experiment, we manipulated the density and spatial arrangement of empty pupal cases and living prepupae, and established appropriate controls for the manipula- tions. Our results suggest that caddisfly aggregations influence both passive accumulation of individuals and species, and alter the nature of interspecific inter- actions in benthic communities.
Materials and methods Fig. 1. (a) Density of aggregated caddisflies based on 52 mm by 23 mm samples (n = 10 for each species) taken from the centres of large aggregations. Error bars represent standard error. High densities are due in part to multiple layers of The study site was in a third-order section of the individuals. (b) Frequency of occurrence of aggregations of caddisflies on substrates (cobbles and boulders) in random- LaPlatte River in Northern Vermont. The LaPlatte is a walk transects consisting of 10 substrates (n = 7 transects). productive stream draining a mixture of agricultural, Error bars represent standard error. forested and suburban areas. The stream bordered an old field and a woodlot with overhanging canopy. Stream depth ranged from 5 to 60 cm and substrates the dominant aggregation-forming species encoun- consisted of sand, silt, pebbles, cobbles and boulders. tered at our field site. Small, geologically diverse boulders (20–40 cm diame- ter) occupied most of the stream bed.
Separate case-addition experiments for Brachycentrus and Neophylax were carried out. To minimize variance Caddisflies in the genera Neophylax (Trichoptera: caused by non-treatment factors, ceramic fire bricks Uenoidae) and Brachycentrus (Trichoptera: Brachyc- (52 × 90 × 23 mm) were used as experimental sub- entridae) are common and widespread in North Amer- strates. Fire bricks are chemically inert and similar in ica (Flint 1984; Wiggins 1998). During spring, larvae of texture to many of the natural boulders and cobbles at both genera form aggregations on the undersides and the site. For each case-addition experiment, 10 repli- vertical surfaces of boulders and cobbles. Once aggre- cates of the following five treatments were established: gated, Brachycentrus larvae immediately pupate, and (1) plain-brick control; brick without cases or glue; (2) adult caddisflies emerge in early spring (Flint 1984). In glue control; spots of glue were applied to the brick end contrast, most Neophylax species enter a prepupal dia- (to measure effects of glue); (3) low density aggrega- pause beginning in mid spring to mid summer and last- tion; caddisfly cases distributed uniformly across the ing up to six months. Pupation occurs in late summer, brick surface; (4) low-density clumped treatment; the and adults emerge in early autumn (Beam & Wiggins same number of cases were used as in treatment 3, but 1987; Martin & Barton 1987). Empty Neophylax cases attached in two high-density clumps (to separate persist in the environment for weeks (Martin & Barton effects of total case number from case density); and (5) 1987) to months (personal observation) after adult high-density aggregation; caddisfly cases were attached © 2003 British emergence. Empty Brachycentrus cases do not persist to the entire end-surface of the brick (Fig. 2). For the Ecological Society, Journal of Animal for more than a few weeks and are relatively rare by Neophylax experiment only, a sixth treatment was Ecology, 72, comparison to Neophylax cases (Fig. 1). Neophylax added; live caddisfly prepupae were attached at high 1015–1026 fuscus (Banks) and Brachycentrus apalachia (Flint) were density to the brick end. The densities used were within
1017 approximately 1 m. The Neophylax experiment began Caddisflies on 24 July 1996 and ended on 14 September 1996. The facilitate benthic Brachycentrus experiment ran from 21 May 1997 until colonization 23 June 1997. The timing of the experiments coincided with occurrence of natural aggregations of each cad- disfly species. All macroinvertebrates were collected from the treated ends of the bricks following the experiment. Beginning at the downstream end of the experimental array, samples were collected in an upstream direction to minimize disturbance of substrates prior to collec- tion. A downstream net was not used because it would have sampled invertebrates from the untreated surfaces of the bricks (McAuliffe 1984). Loss of mobile inverte- brates was minimized by stretching a latex glove over the treated surface of each brick before it was lifted from the streambed. All material from the treated brick surfaces was removed using razor blades (to cut the glue) and scrubbing brushes. Each sample was placed in a 145-µm sieve and rinsed to remove fine sediment before adding 95% EtOH. Immediately following the experiments, macroinver- tebrate samples were collected from 20 haphazardly Fig. 2. Aggregation treatments applied to the small surfaces selected boulders that contained aggregations of the of bricks: (a) control, (b) glue control, (c) low total density, target trichopteran species. A wooden template was (d) low total density clumped, (e) high total density, (f) high used to ensure that the area sampled was equal to the total density live prepupae (Neophylax experiment only). area of a brick end and therefore comparable to our experimental samples. To ensure a valid comparison to the natural range observed at the site. Throughout the experimental aggregations, natural aggregations smaller paper the treatments are referred to as follows: (1) con- than the template were rejected. Natural aggregation trol; (2) glue control; (3) low density; (4) clumped; (5) densities were calculated from these samples (Fig. 1a). high density; and (6) live. Following the Neophylax experiment, we counted For both experiments, caddisflies from prepupal Neophylax prepupae, pupae, and empty cases as well as aggregations were collected from the experimental site empty Brachycentrus cases on 70 cobbles to assess the 2 weeks prior to the experiment. All larvae and pupae frequency of aggregation occurrence in the stream were removed from the cases used for the manipula- (Fig. 1b). The substrates were selected haphazardly tions. Each case was examined under a dissecting from seven random-walk transects. We defined aggre- microscope, and any attached macroinvertebrates were gations as containing groups of five or more cases. removed. The cases were then dried for 48 h and Average aggregation size (sum of prepupae, pupae and attached with silicone glue to brick surfaces. Live empty cases) was 30 for Neophylax (n = 36) and 18 for pupae were collected 1 day before the Neophylax experi- Brachycentrus (n = 17; only empty Brachycentrus cases ment. We blotted dry the ventral exterior surfaces of the existed; the next generation of active larvae was not prepupal cases, removed attached macroinvertebrates, included in this analysis). and glued the prepupal cases to the brick surfaces. In addition, we sampled invertebrates from the The pupae were draped immediately with wet paper entire surfaces of 20 haphazardly selected boulders towels and refrigerated until they were transported that lacked trichopteran aggregations. back to the field site, 12 h later. This treatment was not practical for Brachycentrus because of their short pupation period. Substrates in each experiment were arrayed in a Caddisfly pupae and cases added to the treatments single stream run in a randomized-block design. The were counted to confirm that the treatments had per- treated end of each substrate was orientated down- sisted through the experiments, but these counts were stream, which coincides with the orientation of most excluded from our analysis. With the exception of the aggregations at the site (personal observations). Each live treatment in the Neophylax experiment, there was block in our experimental array spanned the width of negligible loss of caddisfly cases during the experi- © 2003 British the stream with treatment position randomly assigned ments (< 5%). An average of 73% of the cases from the Ecological Society, Journal of Animal within blocks. Treatments were not replicated within live pupae treatment persisted through the experiment Ecology, 72, blocks. The distance between substrates within blocks and remained sealed. Of these, 70% contained live 1015–1026 was on average 0·5 m. Blocks were separated by pupae.
1018 Table 1. Hypothetical community responses to experimental addition of a putative facilitator D. J. McCabe & N. J. Gotelli Response of Response of species density species richness Interpretation
00 Null hypothesis +0 Passive sampling (PS) 0+Shifts in relative abundance distribution (RAD) ++ RAD with or without PS
All invertebrates contained in the experimental species richness for each sample. For the smallest sam- samples and natural aggregation samples were identi- ple in each experiment the total number of species in fied and counted. With the exception of chironomids, the sample represented species richness and species invertebrates were identified to the lowest possible density. taxonomic level. We have therefore measured taxon The nine most abundant taxa (summed over the two richness and taxon density but will refer to these met- experiments) were selected for individual analysis. rics as species richness and species density throughout These taxa accounted for more than 90% of the organ- the paper. Analysis of our data at the family level isms collected from each experiment. Although the yielded qualitatively similar results to the finer-level rank abundance of organisms differed between experi- taxonomic analysis presented here. The majority of the ments, the same list of organisms was used in each hydroptilids sampled was at the free-living, early-instar for consistency. To stabilize variances, the total abund-
stage and could not be identified using existing keys. ance and individual taxon abundance data were log10 Later-instar hydroptilids were identified to genus. transformed. Samples from stream boulders and cobbles lack- ing aggregations were split using a Folsom plankton splitter (Wildco, model number 1831-f10 0298). We identified a minimum of 300 randomly selected inverte- In all analyses, the response variables were total abund-
brates to adequately represent the communities on ance (log10 transformed), species density and species these substrates (Vinson & Hawkins 1996). richness. Data sets were analysed first using a , the results of which were highly significant (Table 2). . We therefore proceeded with individual s for log10 (total abundance), species density and species We quantified species counts as species density, the richness. number of species per replicate in each sample. To con- For the community-level response variables, a trol for the effects of abundance on species density, we randomized-block one-way was used to compare also quantified species richness, the number of species all six (in the case of Neophylax) or five (Brachycentrus) per standard number of individuals counted. The dis- treatments. This model assumes that there is no inter- tinction between species richness and species density is action between blocks and treatments (Underwood important in studies of biodiversity, because species 1997). We used a set of orthogonal a priori linear con- density is very sensitive to total abundance, whereas trasts to test the following null hypotheses for each species richness standardizes samples that differ in response variable: (1) that the glue control did not dif- their abundance (Gotelli & Colwell 2001). Separate fer from the plain control; (2) that the low-density analyses of species richness and species density reveal treatment did not differ from the low-density clumped whether facilitation occurs through passive accumula- treatment; (3) that aggregation treatments did not differ tion of individuals, or through changes in the relative from control treatments; and (4) that aggregations of abundance distribution of assemblages with and live Neophylax pupae did not differ from aggregations without caddisfly aggregations (Table 1). of empty cases of similar density. A Monte Carlo simulation similar to rarefaction (Hurlbert 1971; Simberloff 1978) was used to estimate the expected species richness for a given number of ran- domly drawn individuals from each sample. The small- est samples in the Neophylax and Brachycentrus data Because the samples from natural substrates lacking sets contained 32 and 35 individuals, respectively. For aggregations were not collected from a standardized all but the smallest sample in each experiment, we used area, and because surface area of these substrates was software (Gotelli & Entsminger 2001) to sam- not recorded, comparisons of species density and total © 2003 British ple 32 individuals randomly from each Neophylax sam- abundance were not appropriate. Analysis of expected Ecological Society, Journal of Animal ple and 35 individuals from each Brachycentrus sample. species richness, however, was appropriate because Ecology, 72, We repeated this procedure 100 times for each sample collections were standardized to an equivalent number 1015–1026 and used the average number of species as the expected of individuals. A two-way factorial was used to
1019 Table 2. of effects of (a) Neophylax and (b) Brachycentrus aggregations on abundance, species density, and species Caddisflies richness. *P < 0·05, **P < 0·01, ***P < 0·005 facilitate benthic Effect d.f. SS MS F ratio colonization (a) Neophylax Block Abundance 9 0·8 0·09 3·4*** Species density 9 471·3 52·4 6·6*** Species richness 9 36·4 4·0 3·3*** Treatment Abundance 5 2·1 0·43 16·1*** Species density 5 864·4 172·9 21·8*** Species richness 5 42·3 8·5 6·8*** Error Abundance 44 1·2 0·027 Species density 44 348·9 7·9 Species richness 44 54·5 1·2
(b) Brachycentrus Block Abundance 9 0·569 0·06 0·998 Species density 9 130·3 14·5 0·868 Species richness 9 7·0 0·774 0·461 Treatment Abundance 4 3·6 0·9 14·2*** Species density 4 793·4 198·4 11·9*** Species richness 4 21·2 5·3 3·2* Error Abundance 35 2·2 0·06 Species density 35 583 16·7 Species richness 35 59 1·7
evaluate the main effects and interactions of substrate Table 3. of effects of (a) Neophylax and (b) Brachycentrus
type (artificial or natural) and trichopteran aggrega- aggregations on abundance (log10-transformed). ‘Glue control tions (present or absent). Separate analyses were car- vs. control’, ‘Low density vs. clumped’, and ‘Live vs. high density’ are a priori linear contrasts comparing specific treatments ried out for Neophylax and Brachycentrus, with four described in the text. ‘Aggregation vs. control’ is an a priori treatment groups in each analysis: (1) aggregations on linear contrast comparing the mean of the aggregation treat- natural substrates, (2) aggregations on bricks, (3) nat- ments to the mean of the control treatments. Symbols as in ural substrates lacking aggregations and (4) bricks Table 2 lacking aggregations. ‘Bricks lacking aggregations’ Effect d.f. SS MS F ratio included both control treatments. For the ‘aggrega- tions on bricks’ treatment, all aggregation densities (a) Neophylax and spatial arrangements were pooled. Pooling was Block 9 0·78 0·086 3·2** justified because natural aggregations span a wide Treatment 5 2·1 0·42 15·6*** range of densities, and pooled samples fell within the Error 44 1·19 0·027 Glue control vs. control 1 0·23 0·23 7·9** natural range. Low density vs. clumped 1 0·006 0·006 0·21 Live vs. high density 1 0·056 0·056 2·1 Aggregations vs. controls 1 1·84 1·84 67·9*** (b) Brachycentrus Block 9 2·9 0·33 0·69 A followed by a series of nine one-way analyses Treatment 4 22·7 5·7 12·0*** of variance was used to examine the responses of the nine Error 36 17·1 0·48 most common taxa to the treatments. The taxa exami- Glue control vs. control 1 0·093 0·093 0·20 ned were: Chironomidae, early instar Hydroptilidae, Low density vs. clumped 1 0·69 0·69 1·5 Aggregations vs. controls 1 20·2 20·2 42·4*** Oecetis avara (Banks), Aturus carolinensis (Habeeb), Torrenticola rufoalba (Habeeb), Antocha (Osten Sacken) sp., Crustaceans, Torrenticola (Piersig) sp. Nymphs and Hydropsyche (Pictet) sp. (Table 3). In both experiments, abundance in aggrega- tion treatments was higher than total abundance in the two control treatments (a priori linear contrasts; Results Neophylax: P < 0·001, Fig. 3a; Brachycentrus: P < 0·001, Fig. 4a). In the Neophylax manipulation, the glue con- trol had higher abundance than the plain brick control © 2003 British (P = 0·007; a priori linear contrast; Fig. 3a). There was Ecological Society, Abundance Journal of Animal a significant block effect in the Neophylax experiment Ecology, 72, There was a significant treatment effect on abundance only: downstream blocks tended to have higher abund- 1015–1026 in both the Neophylax and Brachycentrus experiments ance than upstream blocks (P = 0·005). 1020 D. J. McCabe & N. J. Gotelli
Fig. 3. Community responses to Neophylax aggregation treatments and controls. (a) Total abundance of macroinvertebrates. (b) Species density or the total number of macroinvertebrate species found on each substrate. (c) Expected species richness (ES) standardized to a standard number of individuals. Bars of identical shading represent treatments with identical total caddisfly case densities. Black bars represent total coverage of the substrate by caddisfly cases. Grey bars represent 50% coverage. White bars represent zero cases. Error bars represent standard error.
density on aggregations of live Neophylax pupae was Species density lower than on aggregations of empty Neophylax cases The effect of treatment on species density was signi- (P = 0·011; a priori linear contrast; Fig. 3b). There was ficant in both experiments (Table 4). As with total also a significant block effect on species density in the abundance, species density in aggregation treatments Neophylax experiment (P < 0·001). was higher than on control substrates (a priori linear contrasts; Neophylax: P < 0·001, Fig. 3b; Brachycentrus: P < 0·001, Fig. 4b). Species density was significantly higher on glue controls than on plain brick controls in Aggregation treatments had highly significant effects on the Neophylax experiment (P = 0·01; a priori linear species richness in both the Brachycentrus and Neophylax contrast; Fig. 3b). In the Brachycentrus experiment, experiments (Table 5). Species richness in aggregation © 2003 British species density was significantly higher in the low- treatments was higher than on control substrates (a Ecological Society, Journal of Animal density treatment in which cases were uniformly dis- priori linear contrasts; Neophylax: P < 0·001; Fig. 3c, Ecology, 72, tributed, than in the low density clumped treatment Brachycentrus: P = 0·014; Fig. 4c). Species richness 1015–1026 (P = 0·011; a priori linear contrast; Fig. 4b). Species was higher on treatments with high-density Neophylax 1021 Caddisflies facilitate benthic colonization
Fig. 4. Community responses to Brachycentrus aggregations and controls. Response variables and symbols are defined in Fig. 3.
cases than on treatments with live pupae attached (a and 6). Interestingly, several taxa of smaller size (free- priori linear contrast; P = 0·01; Fig. 3c). Species richness living hydroptilids, Oecetis avara, Torrenticola rufoalba, was higher in treatments the low-density clumped Brachy- Torrenticola sp. nymphs) were more abundant on high- centrus cases than in the low density treatment without density empty cases than on live pupae (Fig. 5). clumping (a priori linear contrast; P = 0·03; Fig. 4c). Artificial vs. natural substrates Both substrate type (brick or natural) and aggregation Of the nine most common taxa on the artificial substrates, presence or absence had significant main effects on expected five responded significantly to the experimental treat- species richness (two-way factorial ; Table 7). For ments in both experiments (Chironomidae, Oecetis avara, both trichopteran taxa, species richness was higher in Aturus carolinensis, Hydropsyche sp.; one-way ; the presence of aggregations than in their absence Table 6). There were significant treatment effects on regardless of substrate type (Neophylax: P < 0·001, © 2003 British Antocha sp. and Torrenticola sp. nymphs in the Neophylax Fig. 7a; Brachycentrus: P < 0·001, Fig. 7b). In both the Ecological Society, Journal of Animal experiment and on free-living hydroptilids in the Bra- presence and absence of aggregations, natural substrates Ecology, 72, cycentrus experiment. Most taxa were more abundant had higher species richness than did artificial substrates 1015–1026 on aggregation treatments than on controls (Figs 5 (Neophylax: P = 0·02, Fig. 7a; Brachycentrus: P < 0·001, 1022 D. J. McCabe & N. J. Gotelli
Fig. 5. Effects of Neophylax aggregations on abundance of the numerically dominant taxa. Symbols are defined in Fig. 3.
Table 4. of effects of (a) Neophylax and (b) Brachycentrus Table 5. of effects of (a) Neophylax and (b) Brachycentrus aggregations on species density. ‘Glue control vs. control’ and aggregations on expected species richness. ‘Glue control vs. control’ ‘Low density vs. clumped’ are a priori linear contrasts compar- and ‘Low density vs. clumped’ are a priori linear contrasts ing specific treatments. ‘Aggregation vs. control’ is an a priori comparing specific treatments. ‘Aggregation vs. control’ is an linear contrast comparing the mean of the aggregation treat- a priori linear contrast comparing the mean of the aggregation ments to the mean of the control treatments. Symbols as in treatments to the mean of the control treatments. Symbols as in Table 2 Table 2
Effect d.f. SS MS F ratio Effect d.f. SS MS F ratio
(a) Neophylax (a) Neophylax Block 9 457·7 50·9 6·4*** Block 9 36·3 4·0 3·3*** Treatment 5 861·9 172·4 21·6*** Treatment 5 42·6 8·5 6·9*** Error 44 351·5 8·0 Error 44 54·2 1·2 Glue control vs. control 1 58·2 58·2 7·3* Glue control vs. control 1 0·54 0·54 0·44 Low density vs. clumped 1 13·1 13·1 1·6 Low density vs. clumped 1 2·3 2·3 1·9 Live vs. high density 1 120·1 120·1 15·0*** Live vs. high density 1 9·0 9·0 7·3* Aggregations vs. controls 1 665·9 665·9 83·4*** Aggregations vs. controls 1 30·3 30·3 24·6***
(b) Brachycentrus (b) Brachycentrus Block 9 118·6 13·2 0·74 Block 9 6·9 0·77 0·46 Treatment 4 879·1 219·8 12·3*** Treatment 4 21·2 5·3 3·16* Error 36 643·7 17·9 Error 35 58·8 1·7 Glue control vs. control 1 2·45 2·45 0·14 Glue control vs. control 1 1·2 1·2 0·69 Low density vs. clumped 1 130·1 130·1 7·3* Low density vs. clumped 1 8·6 8·6 5·1* Aggregations vs. controls 1 696·2 696·2 38·9*** Aggregations vs. controls 1 11·2 11·2 6·7*
Discussion Fig. 7b). There was no significant interaction between © 2003 British substrate type and aggregation treatment (Neophylax: Ecological Society, Journal of Animal P = 0·54; Brachycentrus: P = 0·49): aggregations increased Ecology, 72, species richness in a similar manner on both natural Our field and natural experiments demonstrated that 1015–1026 and artificial substrates (Fig. 7). both Neophylax and Brachycentrus facilitate invertebrate 1023 Caddisflies facilitate benthic colonization
Fig. 6. Effects of Brachycentrus aggregations on abundance of the numerically dominant taxa. Symbols are defined in Fig. 3.
Table 6. P-values of the and from the individual one- way s testing for treatment effects on the log-transformed abundance of the nine most common taxa on experimental substrates. Taxa are listed in order of decreasing abundance
P-values
Neophylax Brachycentrus Taxon experiment experiment
< 0·001 < 0·001 Chironomidae < 0·001 < 0·001 Free-living Hydroptilidae 0·079 0·001 Oecetis avara < 0·001 < 0·001 Aturus carolinensis < 0·001 0·012 Torrenticola rufoalba < 0·001 < 0·001 Antocha sp. 0·029 0·386 Torrenticola sp. nymphs < 0·001 0·195 Crustaceans 0·365 0·323 Hydropsyche sp. < 0·001 < 0·001
colonization. Whereas previous studies focused on the proximate and ultimate mechanisms of trichopteran aggregation (Otto & Svensson 1981; Gotceitas 1985; Martin & Barton 1987), no study that we are aware of has examined the effects of trichopteran diapause aggre- gations on the benthic invertebrate community. Fixed retreats (as distinct from mobile cases of many tricho- pterans) of hyropsychid caddisflies have been demon- Fig. 7. Effects of aggregations on expected species richness © 2003 British strated to increase local mayfly abundance (O’Connor (ES) on both natural and artificial substrates. (a) Effects of Ecological Society, Neophylax aggregations. (b) Effects of Brachycentrus aggregations. Journal of Animal 1993) and invertebrate diversity (Diamond 1986). Squares represent artificial substrates (bricks); circles represent Ecology, 72, Cardinale et al. (2002) demonstrated that interspecific natural substrates (cobbles and small boulders; error bars represent 1015–1026 facilitation among caddisfly species enhanced ecosystem standard error.). 1024 Table 7. Two-way factorial testing for main effects of system-wide diversity would require experiments in D. J. McCabe & substrate type and presence or absence of aggregations. The multiple streams as well as natural comparisons among N. J. Gotelli two levels of the substrate factor are artificial and natural. The streams. second factor is presence or absence of aggregations. ‘Controls’ are natural and artificial substrates lacking caddisfly aggregations. Whether caddisflies are important facilitators in a Both glue controls and bare brick controls are included in the given stream depends on a number of factors including: artificial substrates. ‘Aggregations’ represent all artificial the taxa present, the densities achieved during dia- aggregation treatments as well as samples taken from natural pause, and the disturbance regime. Not all caddisflies aggregations. Symbols as in Table 2 aggregate during pupation although many widespread Effect d.f. SS MS F ratio taxa do (examples: Neophylax, Brachycentrus, Glossossoma and Agapetus). Natural disturbance would determine (a) Neophylax how long the aggregations persisted in a particular stream. Aggregation 1 62·1 62·1 32·3*** Thus facilitation by caddisflies is to some degree Substrate 1 10·7 10·7 5·6* context-dependent, but aggregation-forming species Aggregation × substrate 1 0·7 0·71 0·31 Error 92 176·7 1·9 are sufficiently common that their impacts on commu- nity dynamics should be considered in most freshwater (b) Brachycentrus communities. Aggregation 1 16·5 16·5 7·6** Substrate 1 44·9 44·9 20·8*** Aggregation × substrate 1 1·0 1·0 0·47 Error 86 185·2 2·2 The general mechanisms of facilitation discussed com- monly in the literature include resource enhancement functioning. Englund (1993) and Englund & Evander (O’Connor 1993; Power 1990), habitat amelioration (1999) found that caddisfly nets facilitated chironomid and associational defences (Bertness & Callaway 1994; colonization, and Poff & Ward (1988) reported that Stachowicz 2001). The specific mechanisms of facilita- baetid mayflies colonized still-occupied mobile cases tion are diverse and vary by study system. Previous of Glossosoma (Trichoptera: Glossosomatidae). These studies of facilitation in aquatic communities have studies demonstrate that caddisfly retreats and cases implicated substrate stabilization (Fager 1964; have important habitat value, even when active, feeding O’Connor 1993), increased habitat heterogeneity or and sometimes predacious (Englund & Evander 1999) complexity (Botts et al. 1996; González & Downing caddisfly larvae are present. Diapause aggregations may 1999; Horvath et al. 1999), removal of sediment (Power have even greater habitat value because the immobile 1990), accumulation of benthic organic matter caddisflies are neither predacious nor territorial. (Horvath et al. 1999), provision of prey refuges (Gallagher Facilitation of benthic invertebrate colonization has et al. 1983) and hydrodynamic changes (Cardinale also been well documented in marine (Fager 1964; et al. 2002) as the direct mechanisms of facilitation. Gallagher et al. 1983; Gosselin & Chia 1995) and fresh- With the likely exception of sediment removal, all the water environments (Diamond 1986; Englund 1993; factors listed above have potential as mechanisms for Stewart et al. 1999). A series of studies on zebra mussels facilitation in caddisfly diapause aggregations. How- (Dreissena polymorpha) has revealed their importance ever, without additional data, it would be difficult and as facilitators of benthic invertebrates (Botts, Patterson speculative to narrow the list further. In this case we & Schloesser 1996; González & Downing 1999; Horvath, can say, based on the positive response of species rich- Martin & Lamberti 1999; Bially & MacIsaac 2000). ness to caddisfly cases (Figs 3 and 4), that the facilita- These observations and the results of our experiments tive effect is not simply due to passive sampling of a suggest that positive interactions among freshwater larger number of individuals from the community. The species may be ubiquitous. observed response is non-random and could result Caddisfly larvae fit the definition of an ecosystem from differential settling, mortality, emigration, species engineer because case construction assembles particles interactions or a combination of these factors. from the environment into a new form (Lawton & Jones 1995) and alters their habitat value for periphy- ton (Bergey & Resh 1994). When caddisfly cases are aggregated they alter stream substrate texture, which An obvious criticism of artificial substrates is that they affects species richness (Downes et al. 1998; Downes are ‘unrealistic’ and cannot be compared to natural et al. 2000) and species density (Hart 1978) of stream substrates (Rosenberg & Resh 1982; Casey & Kendall invertebrate communities. When cases of the species we 1996). Although our data demonstrate that bricks do examined are aggregated, macroinvertebrate abundance not accumulate as many species as natural stream sub- (Figs 3a and 4a; Table 3) and diversity (Figs 3b,c, 4b,c) strates (Table 7; Fig. 7), our interest is not in the effects © 2003 British increase significantly (Tables 4 and 5). Facilitation as of the substrate type, but rather in the effects of cad- Ecological Society, Journal of Animal demonstrated in our experiments is likely to increase disfly aggregations. The lack of a significant interaction Ecology, 72, intersubstrate variance in the community metrics between substrate type and presence of aggregations 1015–1026 measured. To determine whether aggregations affect (Table 7) confirms that the direction and magnitude of 1025 the species richness response to aggregations is consist- merits additional attention (James & Wamer 1982; Gotelli Caddisflies ent between substrate types. & Colwell 2001). Examination of this interplay is par- facilitate benthic ticularly important because facilitators have positive colonization effects on other populations (e.g. Pringle 1985; Pawlik et al. 1991). Positive interactions may be more common in Because abundance increased in response to our aggre- freshwater habitats than was assumed previously and gation treatments (Figs 3a and 4a), increased species merit a closer examination by aquatic ecologists. density would be predicted based on passive accumul- ation alone. However, our analyses of species richness suggest that passive or random accumulation of indi- Acknowledgements viduals alone cannot account for the increased species This research was funded by Vermont EPSCoR and a density in the presence of caddisfly aggregations. An Theodore Roosevelt grant from The American increase in a measure of species richness that is stand- Museum of Natural History. We gratefully acknowl- ardized to a fixed number of individuals is possible only edge Dr J.C. Conroy for identifying a series of mites with a shift in the relative abundances of the organisms from this study and Dr J.S. Sykora for his examination in the community. It is necessary to invoke a non- of adult Neophylax specimens. This project could not random mechanism during or after colonization to have been completed without the help of several Uni- achieve this result. Potential mechanisms include versity of Vermont undergraduate students: K. Baltus, interspecific interactions in the aggregations (including M. Toomey, A. Pitt, J. Wheeler and K. Marvin. predation, competition and facilitation) and selective sampling (caddisfly cases may preferentially accumu- late colonists of certain species). Whether the relative References abundances changed during colonization, or after, it is Andersen, D.C. & MacMahon, J.A. 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