J. N. Am. Benthol. Soc., 2004, 23(4):713-727 O 2004 by The North American Benthological Society

Role of Podostemurn cerato hyllurn Michx. in structuring benthic macroinvertebrate assembf ages in a southern Appalachian river

Institute of , University of , Athens, Georgia 30602 USA

ERIC D. ROMANISZYN~ Department of Entomology, , Athens, Georgia 30602 USA

Abstract. ceratophyllum Michx. has been associated with extremely high secondary pro- duction of benthic macroinvertebrates in open-canopy rapids. We conducted an experiment in the 7*-order Little River, North Carolina, to test whether varying amounts of Podostemum influenced macroinvertebrate abundance, biomass, composition, and functional feeding group structure. The experiment consisted of 3 treatments in which I! ceratophy2lum was completely, partially, or not removed from portions of 4 bedrock outcrops at 2 sites. Macroinvertebrates were sampled at 0,3, and 6 wk post treatment. Complete removal of I! ceratop@llum greatly reduced overall macroinvertebrate abundance and biomass and altered assemblage structure, but had relatively little effect on functional structure. The lack of change in functional feeding group structure was probably a result of the importance of I! ceratophyllum as a substrate for epiphytic algae, and the availability of nearby colonists in undisturbed habitats. We found a strong positive relationship between surface area of Podostemum and total macroinvertebrate abundance and biomass. We estimated that I! cera- tophyllum increased surface area by 3 to 4 times over bare bedrock. Podostemum ceratophyllum in the Little Tennessee River serves as an important habitat supporting high abundance and biomass of macroinvertebrates. Key words: macrophytes, productivity, habitat, surface area, functional feeding groups, filterers, gatherers, scrapers.

Substratum is one of the major factors influ- Cattaneo and Kalff 1980, Gregg and Rose 1982) encing stream macroinvertebrate distribution and increased deposition of detritus (e.g., Gregg and productivity (Hynes 1970, Minshall 1984, and Rose 1982, Sand-Jensen 1998). Aquatic mac- Allan 1995), and the presence of aquatic vege- rophytes in fast-flowing streams are typically tation can have a profound effect on the benthic restricted to slower-flowing habitats (e.g., Justi- fauna (Percival and Whitehead 1929). Aquatic cia americana (L.) Vahl). One notable exception, increase available habitat for macroinver- however, is the , which thrive in tebrates by augmenting surface area (e.g., Cat- open-canopy rapids (e.g., Everitt and Burkhold- taneo and Kalff 1980), alter local hydrology by er 1991). Although the Podostemaceae is pri- decreasing current velocity (e.g., Sand-Jensen marily a tropical family (Philbrick and Novelo 1998, Madsen et al. 2001, Dodds and Biggs 1995), one species, Podostemum ceratophyllum 2002), enhance streambed stability (e-g., Fritz Michx., is found in the eastern US (Philbrick and and Feminella 2003), and provide food resourc- Crow 1983) where it provides a diverse, 3-di- es. Food effects can be either direct consump- mensional habitat for macroinvertebrates (Nel- tion (= herbivory; e.g., Lodge 1991, Jacobsen son and Scott 1962, Parker and Voshell1983). In and Sand-Jensen 1992) or indirect through en- fact, secondary production of filter feeders in I! hanced surface area for epiphytic algae (e.g., ceratophyllum-covered habitats (Grubaugh and Wallace 1995, Grubaugh et al. 1997) is among Present address: Department of Biology, Coastal the highest ever recorded for streams (Huryn Carolina University, PO. Box 261954, Conway, South and Wallace 2000). Carolina 29528-6054 USA. E-mail: [email protected] Grubaugh et al. (1997) found extremely high E-mail address: [email protected] productivity of macroinvertebrates in Podoste- Present address: Science Applications International mum-covered habitats in the Little Tennessee Corporation, 151 Lafayette Dr., Oak Ridge, Tennessee River, North Carolina. Our overall goal was to 37831 USA. E-mail: [email protected] investigate whether varying amounts of I? cera- 714 J. J. HUTCHENSET AL. [Volume 23

TABLE1. Physical characteristics of Iotla and Needmore sites on the Little Tennessee River (data from Gru- baugh et al. 1997 except velocity and temperature).

Parameter 10 tla Needmore Distance from headwater (krn) Catchment area (ha) Elevation (m above sea level) Water-surface slope (%) Mean annual discharge (m3/s) Mean velocity (m/s) Week 0 Week 3 Week 6 Mean bankfull width (m) Mean bankfull depth (cm) Habitat proportions (%) Depositional Podostemum-covered cobble riffle Podostemum-covered bedrock outcrop Mean daily temperature ("C) (8-y recordp Mean annual degree days (8-y recordp Mean daily temperature ("C) during experiment

a Based on temperatures from 2-h interval thermistor recordings at Needmore only

tophyllum influenced macroinvertebrate abun- change functional structure or community com- dance and biomass. We conducted an experi- position because of the maintenance of some ment at 2 of the sites previously studied by Gru- habitat structure. baugh et al. (1997) in which we removed either all P ceratophyllum or all but the basal 2 cm, and Methods followed macroinvertebrate colonization for 6 wk. Podostemum forms a thick mat on stable sub- Study sites strates, and may also form long (>I5 cm) stems during summer. Our treatments were, therefore, We did the study in the Little Tennessee Riv- designed to show how removing the entire er, a 7th-order stream in the Blue Ridge Phys- or just the long stems influenced macro- iographic Province of the southern Appalachian . Specifically, we assessed how l? Mountains (North Carolina, USA). Underlying ceratophyllum removal influenced: 1) abundance geology includes highly weathered crystalline and biomass of total macroinvertebrates, each rock, which results in low ionic concentrations functional feeding group (FFG), and individual in stream water (Swank and Bolstad 1994). The taxa, 2) proportion of total abundance and bio- 2 study sites, Iotla and Needmore (sites R-2 and mass comprised by each FFG, and 3) commu- R-3, respectively, of Grubaugh et al. 1997; lat nity composition. We hypothesized that com- 35"20f11"N,long 83"31f37"W),were downstream plete removal of P ceratophyllum would dramat- from the confluence of the Cullasaja River and ically reduce total macroinvertebrate abundance the municipality of Franklin, North Carolina. and biomass because of habitat loss. Further, we Needmore was 29 km downstream of Iotla, and expected filter feeders to decline and scraper both sites had narrow, forested floodplains. In abundance and biomass to increase because of the study area, the river passed through the habitat loss and enhanced algal colonization on Nantahala National Forest, which contains scat- newly opened bedrock, respectively. We also tered residences and agricultural fields. Habitats hypothesized that removal of all but the basal I? in both study sites were dominated by cobble ceratophyllum would result in a decline in mac- riffles and bedrock outcrops with dense l? cera- roinvertebrate abundance and biomass but not tophyllum growths (Table 1). Bedrock outcrops extended across most of the river width at estimate surface area of I! ceratophyllum in each Needmore and in large blocks at Iotla. We de- of our samples, and correlated surface area with termined discharge from a US Geologic Survey total macroinvertebrate abundance and biomass gauging station at Needmore and estimated dis- in each sample (see sampling methods below). charge at Iotla from catchment area using linear We calculated Pearson product-moment corre- regression after Grubaugh et al. (1996). lations using log,,(x + 1)-transformed data.

Podostemum remml experiment and surface area Podostemum and rnacroinwtebrate sampling determination We collected one sample from each treatment The experiment, done in the summer of 1997, on each bedrock outcrop on each collection date consisted of 3 treatments in which we complete- using a modified T-sampler (English 1987). The ly (SCRAPE), partially (SNIP), or did not (CON- T-sampler sampled a 103-cmZarea and was fit TROL) remove Z? ceratophyllum from portions of with a 250-pm mesh catchnet. We firmly 4 haphazardly chosen bedrock outcrops within pressed the sampler against the bedrock so that a 100-m reach at each site. We removed all I! the I! ceratophyllum mat formed a seal around the ceratophyllum from a 0.5625-m2 area using putty sampler. We scraped Podostemum and associated knives and wire brushes for the SCRAPE treat- macroinvertebrates inside the sampler from the ment. In the SNIP treatment, we removed all I! bedrock with a putty knife, and preserved all ceratophyllum, except for the basal 2 cm, from a material in 6 to 8% formalin containing a small 0.5625-m2 area using scissors. We did all treat- amount of phloxine-B dye to aid in sample pro- ments on each of the bedrock outcrops, with cessing (Mason and Yevich 1967). each treatment on each outcrop having similar In the laboratory, we washed samples through flows and depths. We measured current velocity nested 1-rnm and 250-pm mesh sieves. We oven for each treatment on each date with a velocity- dried Podostemum retained on the 1-mm sieve at head rod (Wilm and Storey 1944). We began 60°C, and weighed and ashed it at 500°C for 24 treatments and initial macroinvertebrate sam- h to calculate' AFDM. We processed fine benthic pling on 15 July 1997; we repeated sampling 3 organic matter (FBOM) retained on the 250-pm and 6 wk later. We did not sample the SCRAPE mesh sieve similarly to calculate AFDM. How- treatment on week 0 (i.e., the day we removed ever, we undoubtedly underestimated FBOM I! ceratophyllum) because visual and tactile in- because most FBOM is strongly skewed to the spection revealed no I! ceratophyllum or macro- smallest size fractions and may have passed invertebrates on the bedrock after I! ceratophyl- through the sieve (e.g., Minshall et al. 1982). lum removal. Hence, we assumed macroinver- We examined all material retained on the 1- tebrate abundance and biomass and I! cerato- mm sieve at 15x magnification to recover all phyllum standing crop to be 0 for the SCRAPE macroinvertebrates, including careful inspection treatment in Week 0. of macroinvertebrates attached to I! ceratophyl- We estimated the surface area provided by I! lum. We subsampled material retained on the ceratophyllum at our study sites by calculating 250-pm sieve as necessary using a sample split- the surface area of separate parts of Z? cerato- ter (Waters 1969), and removed organisms un- phyllum collected from both sites. We measured der 15X magnification. We identified, counted, stem, root, and apical tip length on a micro- and measured all invertebrates to the nearest scope fitted with an ocular micrometer, and cal- millimeter for conversion to AFDM using taxon- culated surface area of the parts using appro- specific length - mass regressions (Benke et al. priate formulas depending on the shape of the 1999). Taxonomic and FFG assignments fol- part (n = 6 plants). We also determined biomass lowed those of Merritt and Cummins (1996). We (ash-free dry mass [AFDM]) for each part. We identified most insects to genus with the excep- regressed biomass on surface area for each plant tion of Chironomidae, Ceratopogonidae, Empi- using untransformed data, and used this linear didae, and Hydropsychidae. We enumerated the regression equation to predict the amount of Chironomidae as either Tanypodinae or collec- surface area added by I! ceratophyllum at each tor-gatherer Chironomidae. We identified Cera- site using mean standing crops in the CON- topogonidae and Empididae to family. We com- TROL treatments. We also used this equation to bined hydropsychid genera because of difficulty 716 J. J. HUTCHENSET AL. [Volume 23 separating Hydropsyche spp. from early instars added 3.2 to 4.2 m2 (Needmore and Iotla, re- of Cheumatopsyche etrona Ross. spectively) of surface area to each square meter of bedrock. Furthermore, when all samples from Statistical analyses both sites were combined, there was a strong positive relationship between the log,,(x + 1)- We compared log,,(x + 1)-transformed means transformed surface area of I? ceratophyllum and of Podoste~numbiomass, abundance, and biomass the log,,(x + 1)-transformed abundance (R = for total macroinvertebrates, each FFG, and ma- 0.902, p < 0.001, n = 63) and biomass (R = jor taxa statistically among treatments at each 0.887, p < 0.001, n = 63) of total macroinverte- site with repeated-measures analysis of variance brates (Fig. 1). using PROC MIXED (SAS for Windows, version 8, SAS Institute Inc., Cary, North Carolina). We examined significant differences (a = 0.05) Podostemum and FBOM among the 3 treatments using contrast state- ments. We compared the mean arcsin-square At both sites, I? ceratophyllum standing crop in root transformed proportions of individual the SCRAPE treatment was lower than the FFGs (from the 5 and 27 August 1997 samples) CONTROL and SNIP treatments (Fig. 2). At among treatments using PROC GLM (SAS for Needmore, this difference was significant (p 5 Windows). We did not include shredders in FFG 0.001), but the CONTROL and SNIP treatments analyses because they composed 11% of mean were not significantly different (p = 0.104). Oth- total abundance and biomass on all dates except er statistical analyses comparing Podostemum for one, when they composed 9.8% of total bio- biomass among treatments could not be com- mass. We assessed significant differences pleted using PROC MIXED because conver- among treatments for individual FFG propor- gence criteria were not met or because of prob- tions using Tukey's method. lems with infinite likelihood. FBOM composed We used ordination to examine assemblage <5% of total organic matter in the CONTROL structure in each treatment at both sites. We did and SNIP treatments (Fig. 2). FBOM biomass nonmetric multidimensional scaling with PC- ORD for Windows (MjM Software, Gleneden tended to be lowest in the SCRAPE treatment, Beach, Oregon) to ordinate the log,,(x+ 1)-trans- but composed a higher proportion of total bio- formed abundance and biomass for all taxa (n mass (i.e., mean = 14-22%) than the other treat- = 22 and 21, for Needmore and Iotla, respec- ments. Differences in FBOM among treatments tively) that appeared on at least 2 dates for any were not assessed statistically because of low treatment. We used the Sorensen distance mea- standing crops (i.e., <9 g AFDM/m2) relative to sured as % dissimilarity for our analyses. We Podostemum. assessed significance of each axis using a Monte Carlo test, and assessed variation described by distances in the ordination space relative to the Abundance and biomass of total macroinmrtebrates original, unreduced space by calculating a co- and FFGs efficient of determination (McCune and ~efford 1997). There was a significant treatment effect on abundance and biomass of total macroinverte- brates and all FFGs at both sites (all p < 0.001; Results Fig. 3). Multiple comparisons indicated that the Current velocity was similar among treat- abundance and biomass of total macroinverte- ments (Table 1). Discharge declined during the brates and all FFGs were significantly lower in study period, causing a slight reduction in ve- the SCRAPE treatment than in either the CON- locity. TROL or SNIP treatments. The only significant A strong positive relationship (R2 = 0.951, p difference noted between CONTROL and SNIP = 0.001) existed between the surface area of I? treatments was for total biomass at Needmore. ca-atophyllum and its biomass. Using this rela- Significant Date and Treatment x Date interac- tionship (surface area in mm2 = 46.68 + tion effects also were found at Needmore and 13,580.1 X biomass in g AFDM) I? ceratophyllum Iotla (all p < 0.05), except for predator biomass. Podostemum surface area (cm2 ) per sample FIG. 1. Scatter plots of Podostemum ceratophyllum surface area in each sample versus total macroinvertebrate abundance (A) and biomass (B) in each sample.

Proportions of each FFG and the CONTROL treatments, and between the SCRAPE and SNIP treatments (Tables 2,3). Gatherers (n = 9 taxa), scrapers (n = 6 taxa), Chironomids and hydropsychids dominated and filterers (n = 5 taxa) contributed the most to total abundance at both sites (Fig. 4). Filter- (>69%) the total abundance of each treatment ers, especially at Iotla, always dominated bio- at Iotla (Table 4). At Needmore, the relative mass. At Needmore, the proportion of gatherers abundance of the top 5 individual taxa was was lowest in the SCRAPE treatment. The pro- more similar between the CONTROL and SNIP portion of FFG abundance and biomass was treatments compared to the SCRAPE treatment generally similar among treatments. (Table 4). For example, Baetis and Simulium dominated in the SCRAPE treatment, whereas chironomids declined relative to CONTROL Individual macroinvertebrate taxa and SNIP. Hydropsychidae dominated biomass All of the major taxa differed significantly in in the CONTROL and SNIP treatments at both abundance and biomass between the SCRAPE sites while chironomids, Baetis, and hydro- J. J. HUTCHENSET AL. [Volume 23

+ CONTROL A 4 SNIP -v- SCRAPE

Week FIG. 2. Mean (?I SE) standing crops of Podostemum ceratophyllurn and fine benthic organic matter (FBOM) at Needmore (A) and Iotla (B). psychids were important in the SCRAPE treat- greatly reduced total macroinvertebrate abun- ment. dance and biomass. Furthermore, macroinver- tebrate abundance and biomass showed little re- Community composition covery after 6 wk, presumably because of poor l? Community structure in the SCRAPE treat- regrowth of ceratophjllum in the SCRAPE ment differed from the other treatments at treatment. Removal of all but the basal 2 cm of l? Needmore for both abundance and biomass ceratophyllum did not significantly reduce total (Fig. 5), primarily because of the ordination macroinvertebrate abundance or biomass. Total scores for Antocha and Micrasema. At Iotla, how- abundance and biomass in the SNIP treatment ever, only the SCRAPE treatment for biomass tended to be lower than in the CONTROL treat- ment at both sites, but only biomass at Need- was different from the SNIP and CONTROL treatments (Fig. 5), which was caused by scores more was significantly different. These data suggest the basal portion of P ceratophyllum pro- for Anfocha, Empididae, and Hydroptila. Axes 1 vides important habitat and promotes benthic and 2 were significant (p = 0.05) for each ordi- macroinvertebrate productivity in the Little Ten- nation, and accounted for 82.9 to 97.5% of the nessee River. Grubaugh and Wallace (1995) and total variation in abundance and biomass. Grubaugh et al. (1996, 1997) reached similar conclusions for both the Little Tennessee River Discussion and the Oconee River, Georgia. Eflects on total macroinvertebrate abundance and biomass Efects on macroinvertebratefunctional structure Complete removal of P ceratophyllum from Contrary to our prediction, we did not ob- bedrock habitats in the Little Tennessee River serve a strong shift in functional structure re- Needmore

Abundance Biomass - CONTROL SNIP - SCRAPE

M

1 Abundance 1 Biomass

Functional feeding group FIG. 3. Mean abundance and biomass of total macroinvertebrates and each functional feeding group across all dates at Needmore and Iotla. SCR = scrapers, SHR = shredders, GATH = collector-gatherers, FILT = collector-filterers, PRED = predators. lated to the complete removal of I! ceratophyllum. large numbers of diatoms on the leaf and stem We expected the proportion of filterers to de- surfaces of I! ceratophyllum. Thus, diatoms on I? crease because of the reduction in potential at- ceratophyllum provide a valuable food resource tachment sites for filtering, and scrapers to in- for scrapers, which we underestimated. Second, crease because of the increased availability of SCRAPE treatments were potentially colonized open bedrock surface for algal growth. Al- by macroinvertebrates inhabiting undisturbed though there were some signs of this functional adjacent P ceratophyllum. Invertebrates could shift, overall functional structure remained rel- crawl or drift to the newly exposed surfaces, as atively similar among treatments. For example, seen in many studies (see reviews by Wallace the proportion of scraper biomass increased sig- 1990, Mackay 1992). Random colonization of the nificantly in the SCRAPE treatment at Need- SCRAPE treatment by macroinvertebrates from more but the proportion of filterer biomass did surrounding areas would result in FFG propor- not change. Furthermore, there were no signifi- tions similar to the CONTROL treatment. Func- cant differences among treatments in the pro- tional structure may have been more affected if portion of any FFG at Iotla. We offer 2 hypoth- we had removed all Podostmum in a reach, eses to explain this result. First, the stems and which would have virtually eliminated recovery leaves of I! ceratophyllum provide an extensive by crawling during the experimental period. surface area for algal colonization. We observed Large-scale disturbances affecting entire J. J. HUTCHENSET AL. [Volume 23

Needmore

loo] Abundance Biomass -CONTROL SNIP -* a SCFL4PE

- - -0 lotla Abundance 1 Biomass T

Functional feeding group FIG. 4. Mean proportion of total abundance and biomass of each functional feeding group at Needmore and Iotla. Asterisks denote a significant treatment effect and different letters represent significant differencesamong individual treatments (a = 0.05). SCR = scrapers, SHR = shredders, GATH = collector-gatherers, FILT = collector-filterers, PRED = predators. streams or reaches often have greater effects on community composition. As a result, the pri- the benthos because recovery can depend on mary response of completely removing F? cera- distant colonists (Resh et al. 1988, Mackay 1992). tophyllum was a conspicuous overall drop in abundance and biomass across most taxa, but Efjrects on macroinvertebrate taxa not a major shift in community composition across all dates. All of the major taxa were reduced by com- plete removal of F? ceratophyllum. Overall com- Influence of macrophytes on aquatic munity composition was also different in the nzacroinvertebrates SCRAPE treatment compared to the CONTROL and SNIP treatments, although this difference Podostemum is clearly an important determi- appeared to be a result of scores for a few taxa. nant of macroinvertebrate production in the Lit- Few differences were noted between CONTROL tle Tennessee River. Macrophytes can increase and SNIP treatments for major taxa or overall macroinvertebrate populations by providing , 20041 PODOSTEMUMAND BENTHIC MACROINVERTEBRATES 721

TABLE2. Results from repeated-measures analysis of variance for major macroinvertebrate taxa abundance and biomass at Needmore. Data were log,,(x + 1) transformed.For multiple comparisons, different superscript letters denote significant differences among treatment levels using contrasts. C = CONTROL, SN = SNIP, SC = SCRAPE. For other significant effects, D = significant Date effect (p < 0.05), T X D = significant Treatment X Date interaction effect (p < 0.05). Treatment and Date main effectshad df = 2,9, whereas the Treatment X Date interaction effects had df = 4,9.

Multiple Other significant Parameter Taxon F-value p-value comparison effects Abundance Baetis spp. Promresia sp. Chironomidae Serratella spp. Hydropsychidae Simulium spp. Biomass Baetis spp. Promresia sp. Chironomidae Serratella spp. Hydropsychidae Simulium spp.

habitat (= surface area), refuge from predation, Primarily, I? ceratophyllum creates habitat for substrate for epiphytic algae, and food resources benthic macroinvertebrates, especially filter (Minshall 1984, Newman 1991). There is no ev- feeders, through an increase in surface area idence that invertebrates consume I? ccevatophyl- available for colonization. Its highly branched lum tissue in the Little Tennessee River (Rosi- growth morphology supplies 3.2 to 4.2 m2 of Marshall and Wallace 2002). However, I? ccevato- extra surface area to bedrock habitats at Need- phyllum does provide extra surface area for algal more and Iotla, respectively. Hence, I! cerafo- colonization, which provides additional food for phyllum enhances bedrock habitat area for mac- scrapers. roinvertebrates by about 3 to 4X in this river

TABLE3. Results from repeated-measures analysis of variance for major macroinvertebrate taxa abundance and biomass at Iotla. Data were log,,(x + 1) transformed. Different superscript letters denote significant dif- ferences among treatment levels using contrasts. C = CONTROL, SN = SNIP, SC = SCRAPE. For other sig- nificant effects, D = significant Date effect (p < 0.05), T x D = significant Treatment X Date interaction effect (p < 0.05). Treatment and Date main effects had df = 2,9, whereas the Treatment X Date interaction effects had df = 4,9.

Multiple Other significant Parameter Taxon F-value p-value comparison effects Abundance Baetis spp. Promoresia sp. Chironomidae Oligochaeta Hydropsychidae lso~ychiasp. Biomass Baetis spp. Promoresia sp. Chironomidae Oligochaeta Hydropsychidae Isonychia sp. J. J. HUTCHENSET AL. [Volume 23

TABLE4. Proportion (%) of mean total abundance (no./m2) and biomass (mg AFDM/m2) of the dominant 10 macroinvertebrate taxa for each treatment at Iotla and Needmore.

Abundance Control Snip Scrape Iotla Chironornidae 44 Chironomidae 36 Chironomidae Hydrops ychidae 31 Hydropsychidae 33 Hydropsychidae Oligochaeta 6 Oligochaeta 11 Antocha Promoresia 5 Hydracarina 4 Hydracarina Hydracarina 4 Promores ia 4 Baet is lsonychia 3 lsortychia 3 Brachycenf rus Baef is 2 3 Oligochaeta Turbellaria 2 Baetis 2 Promoresia Brachycentrus 1 Stenomma 2 Hyd ropt ila Hydroptila 1 Tanypodinae 1 Empididae Total = 77,002 Total = 59,342 Total = 9579 Needmore Chironomidae Chironomidae 28 Baetis Baet is Baetis 22 Simulium Promoresia Promoresia 17 Chironomidae Hydropsychidae Hydropsychidae 13 Hy dropsychidae Simulium Simulium 12 Promoresia Serratella Serratella 4 Hydracarina Hydracarina Hydracarina 1 Serratella Turbellaria Turbellaria 1 Micrasema Tanypodinae Tanypodinae 1 Antocha Lepidos f oma Oligochaeta <1 Tanypodinae Total 96,507 Total = 77,673 Total = 11,482 depending on the time of year. This surface area partial removal of surface biofilm as well as estimate is conservative, however, given that it plant removal. The Podostemaceae require a only considers standing stock biomass and not surface biofilm for attachment in very rapidly net primary productivity. Regardless, we found flowing areas (Jager-Zurn and Grubert 2000). a strong positive relationship between surface They attach to thread-like substances found in area of Podostemum and total macroinvertebrate cyanobacteria and extracellular polymeric sub- abundance and biomass. Overall, our results stances in biofilms using adhesive hairs. Devel- support previous findings that additional sur- opment of a thick, physically complex, surface face area created by aquatic plants can be a crit- biofilm on inorganic substrates can occur in -3 ical factor for determining abun- wk and depends on current velocity (Battin et dance in estuaries and coastal marine systems al. 2003). Thus, the partial removal of biofilm, (Orth et al. 1984, Hall and Bell 1988, Fredette et coupled with its importance as an attachment al. 1990), lakes (Cyr and Downing 1988, Brown matrix, could have contributed to the slow re- and Lodge 1993), and streams (Glime and Cle- establishment of Podostemum. mons 1972, Minshall 1984, Lee and Hershey The ability of E! ceratophyllum to facilitate high 2000). macroinvertebrate productivity is similar to the Some additional factors may have contributed ecological roles played by bryophytes and the to the strong effects observed in the SCRAPE filamentous alga Cladophora. Thick growth of treatment. The 6-wk duration of each experi- mosses provides a substantial 3-dimensional ment may have not provided enough time for habitat atop hard surfaces for macroinverte- significant regrowth or re-establishment of E! brates (e-g., Glime and Clemons 1972, Suren ceratophyllum and subsequent invertebrate colo- 1991, Stream Bryophyte Group 1999). Similarly, nization. The SCRAPE treatment resulted in the Cladophora mats support a dense macroinverte- 20041 PODOSTEMUMAND BENTHIC MACROINVERTEBRATES 723

TABLE4. Extended.

Biomass Control Snip Scrape

Hydropsychidae Hydropsychidae Hydropsychidae Isomjchia Is0 ychia Chironomidae Chironomidae Chironomidae Brachycentrus Brachycentrus Promo~esia Hydroptila Promoresia Brachycent rus Promoresia Perlesta Perlesta Antocha Serratel la Turbellaria Empididae Baet is Serratella Bae t is Hydroptila Baetis Turbellaria Turbellaria Oligochaeta Hydracarina Total = 10,254 Total = 5964 Total = 862

Hydropsychidae Hydropsychidae Hy dropsychidae Paragnetina Serratella Baetis Baetis Baet is Simulium Serratel la Promores ia Chironomidae Promoresia Paragnetina Serratella Chironomidae Chironomidae Prommesia Corydalus Simulium Micrasema Perlesta Perlesta Antocha Simulium Drunella Hydracarina Brachycentrus Turbellaria Perlodidae Total = 4730 Total = 2778 Total = 252 brate community (Dodds and Gudder 1992, sediment-dwelling taxa (i.e., Trichoptera, Biv- Creed 1994). Bryophytes and Cladophora also alvia, and Nematoda) were insensitive. Our serve as a substrate for epiphytic algae, which study found pronounced effects on all major can serve as food for grazing invertebrates taxa regardless of mobility, perhaps because (Dodds 1991, Dodds and Gudder 1992, Suren our scraping treatment (100% biomass remov- and Winterbourn 1992). FBOM trapped in these al) was more severe than the manual cutting of mats also provides food for gatherers (Glime plants (8447% biomass removal) in Kaenel et and Clemons 1972, Dodds 1991, Suren and Win- al. (1998). The Podostemum examined in our terbourn 1992). Although the standing crops of study grew on bedrock outcrops, which al- FBOM were low in our experiment, this material lowed for their complete removal, unlike the likely turns over rapidly and serves as a food Ranunculus fluitans Lam. and Myriophyllum spi- resource in Podostemum mats. Clearly, the eco- catum L. removed from sand and fine-gravel logical role of Podostemum, bryophytes, and Cla- habitats in the Swiss streams. Thus, sediment- dophora in streams is much greater than their productivity alone. dwelling taxa were not entirely eliminated by Kaenel et al. (1998) found pronounced short- the macrophyte treatment in Kaenel et al. term negative effects on total macroinverte- (1998). Kaenel et al. (1998) also found that the brate abundance in 2 Swiss lowland streams abundance of macroinvertebrates recovered after experimental reductions of plant biomass. within 4 to 6 mo. We do not know the length Taxa that depended on macrophytes for habitat of time needed for recovery of macroinverte- (i.e., Simuliidae, Chironomidae, and Hydracar- brate abundance and biomass in the Little Ten- ina) were especially sensitive to plant removal, nessee River, but suspect it depends on the re- whereas highly mobile taxa (i.e., Baetis) and covery of I! ceratophyllum. J. J. HUTCHENSET AL. [Volume 23

Needmore 2 Abundance Biomass 'I v % v om v

I

Abundance Biomass

. 0 v 00 0.0 v 0. v CONTROL v 0 SNIP v SCRAPE

1

Axis 1 FIG. 5. Ordination plots of the first 2 axes from nonrnetric multidimensional scaling analyses of each treat- ment based on the abundance and biomass of taxa that appeared on at least 2 dates for any treatment at Needmore and Iotla.

Role of Podostemaceae in stream ecosystems in the Yellow River, Georgia (Krieger and Bur- banck 1976). In addition to habitat for inverte- The Podostemaceae are distributed widely brates, presence of Z? ceratophyllum occasionally and play a variety of important roles in streams is associated with certain fish species such as worldwide. Wuillot (1994) found very high spe- cies richness and density of Baetidae in the erect the riverweed darter Etkostoma podostemone Jor- stems of Podostemaceae in the River Niandan, dan (Jenkins and Burkhead 1994, Connelly et al. Guinea. In 3rd- and 4th-order streams of Costa 1999). The high densities of stream invertebrates Rica, dense mats of Marathrum (Podostemaceae) in I? ceratophyllum mats probably serve as a valu- supported extremely high densities of caddis- able prey resource for benthos-feeding fish. For flies and predatory Corydalus, and provided ovi- example, we frequently observed redhorse suck- position sites for odonates (de la Rosa 1995). ers foraging in the Z? ceratoplyllum beds while One species of caddisfly Brachycentrus etaoakn- we were sampling. An additional ecological val- sis Wallace, is restricted to I? ceratophyllum-cov- ue of Z? ceratophyllum is its importance in detritus ered habitats in the southeastern US (Wallace dynamics because it breaks down rapidly (Hill 1971, Willats 1998). Podostemum mats served as and Webster 1982) and can contribute a season- a source habitat (sensu Pulliam 1988) for the ally important pulse of organic matter to the de- pleurocerid snail, Oxytrema suturalis Haldeman, trital food web in mid-sized rivers (Hill and Webster 1983). Finally, I? ceratophjllurn may be a CREED,R. I? 1994. Direct and indirect effects of cray- useful indicator species of high water quality fish grazing in a stream community. Ecology 75: because of its intolerance of siltation and need 2091-2103. for high concentrations of dissolved oxygen CYR,H., AND J. A. DOWNING.1988. Empirical relation- (Meijer 1976, Philbrick and Crow 1983, Philbrick ships of phytomacrofaunal abundance to plant and Novelo 1995). Our experiment provides ad- biomass and macrophyte bed characteristics. Ca- nadian Journal of Fisheries and Aquatic Sciences ditional evidence for the valuable role of I? cer- 45:976-984. atophyllum in stream ecosystems. DE LA ROSA, C. 1995. Middle American streams and rivers. Pages 189-218 in C. E. Cushing, K. W. Acknowledgements Cummins, and G. W. Minshall (editors). Ecosys- tems of the world: river and stream ecosystems. Sue Eggert and Alonso Ramirez assisted in Elsevier, Amsterdam, The Netherlands. field collections, and Peter Esselman and Mary DODDS,W. K. 1991. Community interactions between Palmer assisted in the laboratory. Karen Block- the filamentous alga Cladophora glomerata (L.) Kuetzing, its epiphytes, and epiphyte grazers. som provided statistical guidance. Wyatt Cross, Oecologia (Berlin) 85:572-580. Alonso Ramirez, Chris Pennuto, David Rosen- DODDS,W. K., AND B. J. E BIGGS.2002. Water velocity berg, and 2 anonymous reviewers provided attenuation by stream periphyton and macro- helpful comments on an early draft. The Na- phytes in relation to growth form and architec- tional Science Foundation (DEB-9632854 and ture. Journal of the North American Benthological DEB-0218001) supported this work through the Society 21:2-15. Coweeta LTER program. JJH also acknowledges DODDS,W. K., AND D. A. GUDDER.1992. The ecology support by the mini-grant program and the De- of Cladophora. Journal of Phycology 28:415-427. partment of Biology, Coastal Carolina Univer- ENGLISH,W. R. 1987. Three inexpensive aquatic Sam- sity. plers for the benthos, drift and emergent fauna. Entomological News 98:171-179. EVERTTT,D. T., AND J. M. BURKHOLDER.1991. 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