loss of riparian vegetation alters the ecosystem role of a freshwater crayfish ( cherax...

Loss of riparian vegetation alters the ecosystem role of a freshwatercrayfish (Cherax destructor) in an Australian intermittent

lowland stream

Darren Giling1, Paul Reich2, AND Ross M. Thompson3

School of Biological Sciences, Monash University, Clayton, Victoria 3800, Australia

Abstract. Loss of riparian vegetation surrounding streams can affect instream biota by altering streamcharacteristics, such as terrestrially derived detrital inputs and instream productivity. Omnivorouscrayfish can be a dominant component of stream biota and are considered a keystone species because oftheir ability to forage at multiple trophic levels. Resource shifts caused by changes in riparian canopy havethe potential to influence crayfish diet and growth. We investigated the effects of changes in canopy coveron the crayfish Cherax destructor in a southeastern Australian lowland stream. We compared the diet of C.destructor between sites with and without riparian cover and determined how differences in the quantity offood resources between sites affected crayfish growth. The availability of basal (plant, algae, and detrital)resources was related to the presence of a riparian canopy. Aquatic macrophytes were more common atsites with no canopy cover and terrestrially derived leaf litter was more abundant at sites with an intactcanopy. Stable isotope and gut content analyses of crayfish diet indicated a shift toward autochthonousfood sources in individuals from sites with no canopy cover. In laboratory feeding trials, crayfish hadhigher growth rates when fed macrophyte material than when fed terrestrially derived leaf litter. Insightsgained into resource use by crayfish, particularly the importance of aquatic invertebrates in crayfish diet,emphasize the merits of conducting both gut content and stable isotope analyses to assess short- andlonger-term aspects of diet. Further structural and functional impacts of changes to riparian conditionshould be investigated, but the trophic role of C. destructor in stream food webs appears to be sensitive toalterations in the dominant basal resources associated with changes in riparian canopy.

Key words: diet, basal resources, restoration, stable isotope, detritus, degradation, yabby.

Stream ecosystems are heavily used by humans andare among the most degraded systems worldwide(Sala et al. 2000). Anthropogenic impacts on streamsinclude removal of woody debris, channel straight-ening, and alteration and removal of riparian vegeta-tion zones (Power et al. 1988). Degradation of riparianzones can affect ecosystem functions, including waterfiltration, bank stabilization, and provision of nutri-ents and organic matter to streams (Junk et al. 1989,Myers and Swanson 1992, Naiman and Decamps1997). Removal of riparian vegetation can alterinstream ecosystem functions, such as C and nutrientfluxes, and disrupt terrestrial–aquatic linkages (Bunnet al. 1999, Dodds et al. 2004, Esslemont et al. 2007).

The major impacts of riparian vegetation removalare a reduction in the amount of terrestrial woody

debris and leaf litter entering streams (Reed et al.1994) and simultaneous elevation of light levels.Increased light facilitates proliferation of filamentousalgae and macrophytes, and shifts the system towardan autochthonous resource base (Feminella et al.1989). This shift can cause considerable changes tostream ecosystems because allochthonous inputs(both dissolved and particulate fractions) often fuelthe food webs of low-order streams (Vannote et al.1980, Wallace et al. 1995). Basal resource shifts altercomposition and trophic structure of aquatic inverte-brate communities and have pervasive effects onstream foodweb structure (Thompson and Townsend2004).

Freshwater crayfish can dominate aquatic inverte-brate biomass in freshwater ecosystems and processlarge amounts of organic matter (Nystrom and Strand1996, Whitledge and Rabeni 1997). Most species,including the focal species of our study, are oppor-tunistic omnivores that consume a wide variety of

1 E-mail addresses: [email protected] [email protected] [email protected]

J. N. Am. Benthol. Soc., 2009, 28(3):626–637’ 2009 by The North American Benthological SocietyDOI: 10.1899/09-015.1Published online: 16 June 2009

626

food sources including detritus, biofilm, algae, mac-rophytes, invertebrates, and fish eggs (Stenroth andNystrom 2003, Dorn and Wojdak 2004). Crayfish thatshred leaf litter increase the surface area available forfurther microbial and macroinvertebrate processingand provide an important pathway for organic matterto reenter the stream food web (Parkyn et al. 1997,Whitledge and Rabeni 1997). Because crayfish feed atmultiple trophic levels, they can affect stream foodwebs through their actions as predators (Momot 1995,Stenroth and Nystrom 2003) and as consumers ofautotrophs (Brooks 1997) or decaying material (Mo-mot 1995, Parkyn et al. 1997). In some cases, crayfishalso are an important dietary resource for native fishspecies (Ebner 2006).

The consequences of riparian clearing and reducedallochthonous material input are well documented forother macroinvertebrate assemblages (e.g., Reed et al.1994, Wallace et al. 1997, Hall et al. 2001, Thompsonand Townsend 2004), but relatively little is knownabout the effects on freshwater crayfish, despite theirrecognized importance in aquatic ecosystems (Parkynet al. 1997). Freshwater crayfish often are overlookedbecause conventional macroinvertebrate samplingmethods provide unreliable estimates of crayfishdensity (Rabeni et al. 1997). Landuse changes canalter the diet and trophic interactions of freshwatercrayfish, and previous research showed that crayfishconsumed less allochthonous material in New Zeal-and streams with no riparian vegetation than instreams with riparian vegetation (Parkyn et al. 2001).Therefore, a plausible hypothesis is that changes inriparian canopy cover in Australia will influence theflow of energy to the native common yabby, Cheraxdestructor (Clark 1936). Allochthonous detrital matteris considered a lower quality food source thanmacrophytes. Thus, crayfish growth rates might beinfluenced by riparian changes (Brooks 1997, Reid etal. 2008b).

Stable isotopes are often used to assess the flow ofenergy in aquatic food webs (Renones et al. 2002,Schindler and Lubetkin 2004, Rybczynski et al. 2008).C and N both exist as 2 stable (nonradioactive)isomers, 12C/13C and 14N/15N (Sulzman 2007). Thechange in isotopic ratios caused by assimilation inorganisms is predictable. Thus, d13C and d15N valuesprovide useful information for tracing passage oforganic matter through food webs (C) and identifica-tion of trophic position (N).

We investigated the effect of riparian cover on thefeeding ecology and trophic interactions of C. destruc-tor in a southeastern Australian lowland stream in anagricultural landscape. The specific aims of the studywere to compare the diets of C. destructor in sites with

high and low canopy cover and to determine how C.destructor growth is affected by alternative foodsources that differ in availability with changes inriparian cover. We hypothesized that C. destructorfrom stream sites with low canopy cover and, hence,less coarse particulate organic matter (CPOM) inputs,would have a greater proportion of autochthonousmaterial in their diet. We expected that C. destructorfed macrophyte diets would accumulate more bio-mass than those fed detrital matter.

Methods

Study sites

We worked in 6 study sites along an 8-km section ofJoyce’s Creek, a 3rd-order lowland intermittent tribu-tary of the Loddon River, near Castlemaine, Victoria(upstream lat 37.17uS, long 143.96uE; downstream lat37.11uS, long 143.96uE). The major land uses adjacentto all sites were predominantly sheep and cattlegrazing with some mixed cropping. Sites representeda contrast between high (closed sites: H1, H2, H3) andlow (open sites: L1, L2, L3) riparian canopy cover.Sites from each category were interspersed along thecreek to avoid longitudinal bias. The dominantriparian overstory species was Eucalyptus camaldulen-sis (river red gum).

At the time of sampling (April and May 2008), thestream was not flowing and each site consisted of anisolated pool. Flow along the stream occurred for atotal of only 77 d during 3 brief periods after January2005. The most recent flow prior to sampling occurredover 2 d in February 2008 (Theiss EnvironmentalMonitoring, Victorian stream gauging network,Gauge no. 407230). On no occasion did streamdischarge exceed historical baseflow (Q90). Thus,transfer of organic matter and biota between siteswas limited before and throughout the study period.

Resource assessment

We quantified resource availability by assessing %

canopy closure, CPOM standing stock, and cover ofmacrophyte species for each pool. We measuredcanopy cover by taking 3 photographs at each site(upstream, center, and downstream of pool) with adigital camera equipped with a hemispherical lens.We analyzed the photographs with Gap LightAnalyser software (version 2.0; Simon Fraser Univer-sity, Burnaby, British Columbia, and the Institute ofEcosystem Studies, Millbrook, New York) and calcu-lated % canopy closure.

We assessed the amount of CPOM at each site byhaphazardly sampling 5 locations on the streambed

2009] RIPARIAN CONDITION ALTERS CRAYFISH DIET 627

with a polyvinyl chloride tube (25-cm diameter). Weremoved all CPOM from the tube by hand and a net(1-mm mesh size). We were unable to samplelocations with water depths .,40 cm with thismethod, but such locations made up a small fractionof the pool area. We washed samples of CPOMthrough a 1-mm sieve to remove fine particulateorganic matter (FPOM) and larger stones or otherinorganic items. We then oven-dried the samples(60uC, 72 h) and recorded dry mass. We estimated thecomposition of the sample (leaves, sticks, bark,reproductive structures, macrophyte material, andanimal feces) visually to the nearest 5%. We com-busted samples (550uC, 4 h) and reweighed them toobtain ash-free dry mass (AFDM)/m2 for eachsample. We measured AFDM to exclude the effectof inorganic components (for example sand) in thesamples.

We estimated % cover of macrophyte species,benthic algae, terrestrial grass (growing within thewet area of the pool), large woody debris, and openwater at the open and closed sites visually to thenearest 5% along transects spaced at 2-m intervalsacross each pool. This estimate allowed us to examinerelative differences in % cover among sites but wasnot intended as measure of primary production.

Gut content analysis

Stable isotope analysis and gut content analysis areused frequently to assess aquatic ecosystems andcrayfish diets, but few studies have used them incombination (but see Whitledge and Rabeni 1997,Hollows et al. 2002, Jones and Waldron 2003, Olssonet al. 2008, Rybczynski et al. 2008). Gut contentanalysis represents a snapshot of crayfish diet andcan underestimate animal matter because it is moreeasily digested than detritus (Whitledge and Rabeni1997, Hollows et al. 2002, Alcorlo et al. 2004). Stableisotope analysis provides an indication of what aconsumer has assimilated, rather than merely ingest-ed, over a longer time period (Rybczynski et al. 2008).However, stable isotope analysis cannot alwaysprovide accurate resolution of prey items if basalresources do not have distinctive C signatures(Hollows et al. 2002, Rybczynski et al. 2008). Wecombined the techniques because of the advantagesand drawbacks of each.

We used fyke nets (6-mm mesh, 80-cm 3 55-cmopening) and unbaited box-traps (3-mm mesh,45 cm 3 25 cm 3 25 cm) set overnight to collect C.destructor from all 6 sites for gut content and stableisotope analyses. We checked traps in the morning,euthanized any C. destructor caught, and transported

them to the laboratory on ice. We collected a total of42 C. destructor for gut content analysis (7 from H1, 2from H2, 8 from H3, 12 from L1, 6 from L2, 7 fromL3). We dissected the stomach from each C.destructor and washed out and diluted the gutcontents. We excluded C. destructor with emptystomachs (5 from open sites, 5 from closed sites)from all further gut content analyses. Thus, we used12 C. destructor from closed and 20 C. destructor fromopen sites.

We identified large or whole items in the gutunder a dissecting microscope before preparingpermanent slides to identify plant and animalfragments in the gut (after Jaarsma et al. 1998,Thompson and Townsend 2005). We filtered a 1-mLsubsample of the diluted gut contents through a0.45-mm nitrocellulose filter and cleared the filter for12 h with cedar immersion oil. We then mountedthe filter in Hoyer’s mountant and dried it at 60uCfor §62 h. We analyzed 8 haphazardly chosen fieldsof view at 4003. Reference slides were used toidentify gut contents into categories: E. camaldulensisCPOM, Typha sp., Triglochin procera, Myriophyllumcrispatum, unidentified macrophytes, chironomids,oligochaetes, unidentified macroinvertebrates, un-identified invertebrate spines, C. destructor, fungalhyphae, diatoms, filamentous algae, and FPOM. Wevisually estimated the percentage of each itemwithin the field of view, and quantified items onscale of 1 to 6 (1 = ,1%, 2 = 1–5%, 3 = 5–10%, 4 =

10–30%, 5 = .30%, and 6 = large objects in gut) toproduce the relative abundance of a particular itemin the guts.

Stable isotope analysis

We collected 42 C. destructor for stable isotopeanalysis. We also collected samples of basal resourcesand macroinvertebrates from 2 study sites, 1 withhigh and 1 with low canopy cover (H1 and L1). Basalresources collected included Typha sp., CPOM, E.camaldulensis, Potamogeton tricarinatus, and T. procera,green filamentous algae (Cladophora), and biofilm(scraped off tiles placed on the streambed for 6 wkto allow biofilm growth). CPOM differed from E.camaldulensis in that it contained large debris from arange of plant species, including macrophytes,whereas E. camaldulensis samples contained only riverred gum leaves and fragments. We collected bothfresh and conditioned Typha, CPOM, and E. camaldu-lensis to assess the potential effect of biofilm growthon stable isotope signature. Material was deemedconditioned if it was in the wet area of the pool andinundated with water. We used a dip net to collect

628 D. GILING ET AL. [Volume 28

macroinvertebrate samples by scooping throughbenthic sediment and the water column. Invertebrateswere collected to represent a range of functionalfeeding groups and included chironomid larvae(collectors), gastropods (grazers), corixids (omni-vores), notonectids (predators), and larval odonates(predators). We kept animals in distilled water for§24 h to void their digestive tracts before stableisotope analysis.

We washed samples for stable isotope analysis indistilled water to avoid contamination. We removed asection of tail muscle from each C. destructor bydissection, dried all the samples at 60uC in an oven for1 wk, and crushed them into a fine powder. Stableisotope analysis was done at the Stable IsotopesAnalysis Laboratory at Griffith University, Brisbane,with an elemental analyzer (Eurovector EA 3000,Milan, Italy) and isotope ratio mass spectrometer (GVIsoPrime, Manchester, UK). Isotope ratios werecompared to standards (Australian National Univer-sity [ANU] sucrose for C, atmospheric N for N), andreported as the isotope ratio in parts per thousand(%).

Laboratory experiment

We used laboratory experiments to investigateeffects of different food sources on the growth rateof C. destructor. We randomly assigned 10 individualsto 1 of 4 food source treatments (Typha sp. stems androots, T. procera stems and roots, E. camaldulensisCPOM [conditioned leaves, sticks, bark], and unfedcontrol).

We collected C. destructor (initial size 20.0–33.0 mm, 4.47–20.09 g wet mass) for the feedingtrials from a single large pool on an adjacent creek(Middle Creek) to obtain the number of individualsin a defined size range required to undertake feedingtrials. Obtaining individuals from a single locationalso reduced potential variability between popula-tions based on past exposure to different potentialfood sources. We trapped animals in fyke nets setovernight and transported them back to the labora-tory at Monash University, Clayton. We kept C.destructor in separate 6-L aquaria filled with 4 L oftap water (conditioned to remove Cl) with no visualcontact to reduce aggressive interactions. We main-tained aquaria in a natural lighting regime (16:8 hlight:dark) at 20uC to avoid winter torpor (Lake andSokol 1986). We fed each C. destructor an identicaldiet of frozen Daphnia and E. camaldulensis CPOM for2 mo before beginning the experiments. One weekbefore commencing feeding trials, we cleaned allaquaria and withheld food to promote feeding

during trials. We collected food sources representingthe most widespread basal resources from the studysites and supplemented these sources with materialfrom a nursery.

On day 0 of the experiment, and every 5 dafterward, we fed C. destructor 20.00 6 0.10 g cleanplant material that was weighed after being blottedand pressed dry with paper towel. Each 20.00 6

0.10 g mass of CPOM contained an approximatelyequal assortment of leaves, small sticks, and bark.Macrophyte food contained similar proportions ofstems and roots, with a mixture of various growthstages and conditioned material. We removed oldplant material from aquaria with a fine net beforeadding new material. We assessed C. destructor growthand biomass production by measuring orbital carapacelength (OCL) and wet mass of each individual on day 0and every 5 d afterward before addition of fresh food.The experiment lasted 40 d.

To assess the processing rate (material consumedby C. destructor or shredded into particles too small tobe netted) of each food source, we carefully removedthe material remaining after the first 5-d interval witha 0.5-mm mesh net, blotted it dry, and reweighed it.Material that had been shredded by C. destructor andwas too small to be netted was considered processedbecause it was available for further microbial break-down and to filter-feeding organisms. We alsomaintained 5 control aquaria per treatment (no C.destructor present) for 5 d to examine mass loss causedby microbial breakdown and leaching of each foodsource and to control for small amounts of materiallost in the drying process.

Data analyses

We compared resource availability between closedand open sites with a single-factor analysis ofvariance (ANOVA). We used a x2 frequency tableto assess the number of C. destructor guts from openand closed sites containing food items (presence/absence) from a simplified category list (algae, E.camaldulensis CPOM, macroinvertebrate, macro-phyte, other). We analyzed stable isotope dual-signature plots for open and closed sites by fittinga Bayesian mixing model with the software packagesiar (stable isotope analysis in R; version 3.2, RFoundation for Statistical Computing, Vienna, Aus-tria). We compared food processing rates with ananalysis of covariance (ANCOVA) model with theinitial mass of the C. destructor as a linear covariate.We used split-plot ANOVA to analyze C. destructorgrowth rates among treatments. We treated individ-ual C. destructor as blocks and experiment day and food


source as factors. We did all statistical analyses in thestatistical software R (version 2.7.0) with a = 0.05.

Results

Site resource assessment

Open and closed sites differed considerably in thetype and amount of basal resources present. Closedsites had significantly greater canopy cover (34.8 6

4.7%) compared with the open sites (4.7 6 2.2%)(Table 1). Significantly more E. camaldulensis CPOMwas present at closed sites (222.65 6 19.19 g/m2) thanat open sites (29.63 6 10.98 g/m2) (Table 1). Macro-phytes comprised significantly more of the CPOM atopen sites (99.68 6 67.78 g/m2) than at closed sites(9.04 6 4.62 g/m2) (Table 1). Total macrophyte coverwas greater at open sites than at closed sites (Table 2).Most notably, % cover of Typha sp. was ,363 greaterat open than at closed sites (single-factor ANOVAwith planned comparison, F1,111 = 73.25, p , 0.001).

Gut content analysis

Stomach contents showed that C. destructor wereomnivorous and that individuals from open sites hadconsumed more macrophyte material than those fromclosed sites (Table 3). Cherax destructor from closedsites had consumed ,23 the amount of E. camaldu-lensis CPOM than those from open-canopy sites. Thenumber of guts containing items from the simplifiedcategory list did not differ significantly between openand closed sites (frequency analysis, x2

= 3.79, df = 4, p= 0.497). These results were not biased by size becauseOCL of C. destructor used for gut content analyses didnot differ between the open and closed sites (separatevariances t-test, t28.49 = 0.220, p = 0.826).

Stable isotope analysis

Dual signature plots showed little variation in Csources or trophic position of C. destructor among sites(Fig. 1A, B). These plots suggested that C. destructor

TABLE 1. Mean (SE; n = 3) % canopy cover, pool characteristics, and mean (SE; n = 5) ash-free dry mass (AFDM) of Eucalyptuscamaldulensis coarse particulate organic matter (CPOM; includes leaves, bark, sticks, and reproductive structures) and macrophyteCPOM (includes Triglochin procera, Typha sp., and other unidentified macrophyte material) at each site (closed high canopy cover:H1, H2, H3; open low canopy cover: L1, L2, L3). Statistical analyses are the results of single factor analyses of variance withplanned comparisons of the closed and open sites. ND = not detected.

Characteristic

Closed Open Statistical analysis

H1 H2 H3 L1 L2 L3 df F p

% canopy cover 44.0 (4.1) 31.6 (2.6) 28.8 (1.7) 7.7 (2.2) 5.9 (1.1) 0.4 (0.05) 1,12 230.56 ,0.001Pool length (m) 34.0 44.0 26.0 28.0 32.0 62.0Pool width (m) 8.0 7.6 7.0 4.4 8.3 11.3Approximate pool

area (m2) 167.4 238.8 137.6 87.2 210.0 419.8Maximum depth (m) 1.1 1.0 1.0 0.7 1.0 1.3E. camaldulensis CPOM

(g AFDM/m2)258.84(58.61)

193.48(92.49)

215.64(48.10)

46.76(12.71)

9.16(3.74)

32.98(32.49) 1,24 21.59 ,0.001

Macrophyte CPOM(g AFDM/m2) ND

15.21(8.13)

11.90(7.51)

232.43(75.52)

9.55(2.64)

57.05(20.37) 1,24 26.06 ,0.001

TABLE 2. Mean (SE) % cover/m2 of macrophytes, woody debris, and open water at each study site (closed high canopy cover:H1, H2, H3; open low canopy cover: L1, L2, L3). ND = not detected.

Type

Closed Open

H1 H2 H3 L1 L2 L3

Potamogeton tricarinatus ND ND ND 13 (4.93) ND NDCladophora ND 0 (0.07) ND 30 (6.97) ND NDTypha sp. 1 (0.26) 1 (0.40) 1 (0.63) 24 (6.48) 55 (7.02) 29 (4.86)Triglochin procera ND 0 (0.04) ND 16 (4.51) 0 (0.10) 0 (0.07)Large woody debris 7 (1.92) 2 (0.64) 0 (0.15) 2 (0.98) ND NDMyriophyllum crispatum ND ND 1 (0.19) ND ND 1 (0.35)Phragmites australis ND ND ND ND ND 9 (1.56)Open water 93 (1.86) 97 (0.65) 98 (0.54) 16 (7.17) 44 (6.93) 60 (5.34)


obtained a large proportion of energy requirementsfrom macroinvertebrates (in particular, the d13C valueof C. destructor is similar to that of gastropods), andother sources, including biofilm, E. camaldulensis, andmacrophytes. Cherax destructor had d13C values(range: 232.3 to 230.8) intermediate to those of otherresources, including invertebrates (d13C range: 237.1to 232.0), biofilm (d13C range: 235.5 to 235.8), andmacrophytes, detritus, and algae (d13C range: 230.1 to224.1). No clear distinction between open and closedsites appears to exist in the suite of resources used byC. destructor. d13C values of basal resources weresimilar for material collected from open and closedsites. Thus, we were unable to ascertain whether theconsumption of allochthonous or autochthonousmaterial differed between open and closed sites.

A stable isotope mixing model confirmed that C.destructor probably obtained C for assimilation from awide range of sources, including E. camaldulensis andTypha sp., but predominantly from macroinvertebrates(proportion = ,0.43 and ,0.65 at closed and open sites,respectively; Fig. 2A, B). The mixing model alsoshowed that E. camaldulensis was less likely tocontribute to the diet of C. destructor at the open thanat the closed site. Cladophora was identified as anotherimportant resource at the open site, whereas other basalresources contributed minor amounts to the diet. Whenjuveniles (,20 mm OCL; Beatty 2006) and adults(§20 mm OCL) were analyzed separately, d13C valuesof juveniles were 1.7% lower than those of adults.

Laboratory experiment

Cherax destructor processed more T. procera thanTypha sp. or E. camaldulensis CPOM over a 5-d period(ANCOVA, post hoc Tukey’s test, F2,25 = 30.68, p ,

0.001; Fig. 3). This result was independent of theinitial mass of each C. destructor used in the feedingtrials (ANCOVA, F2,23 = 0.61, p = 0.550).

Mass gain differed among treatments over the 40-dexperiment. The treatment 3 day interaction effectwas significant (F21,238 = 3.167, p = 0.005; Fig. 4).Therefore, treatment groups were analyzed separatelywith a single-factor ANOVA. Mass of C. destructorincreased significantly over time when fed Typha sp.(ANOVA, F7,238 = 3.586, p = 0.001) and T. procera(ANOVA, F7,238 = 7.951, p , 0.001). Mass of C.destructor did not change over time when fed E.camaldulensis CPOM (ANOVA, F7,238 = 0.639, p =

0.723) or nothing (ANOVA, F7,238 = 0.604, p = 0.752).Eight C. destructor molted during the feeding trial.Molting could have influenced the results because C.destructor become less active and feed less whenmolting.

Discussion

Resource availability

We investigated the effects of riparian canopy coveron the feeding ecology and trophic interactions of afreshwater crayfish by comparing resource availabil-

TABLE 3. Contents of Cherax destructor stomachs from closed and open sites. Occurrence is expressed as % of guts sampledfrom open (n = 20) or closed (n = 12) sites. Abundance was calculated from the percentage of each item within the field of viewand was quantified on a scale of 1 to 6 (1 = ,1%, 2 = 1–5%, 3 = 5–10%, 4 = 10–30%, 5 = .30%, and 6 = large objects in gut).Abundance is expressed as the mean median (SE) score of an item in counts of 8 haphazard microscope fields. Fine particulateorganic matter (FPOM) was recorded as present or absent only. CPOM = coarse particulate organic matter; ND = not detected.

Diet item category Diet item

Closed sites Open sites

Occurrence Abundance Occurrence Abundance

CPOM Eucalyptus camaldulensis 92 1.32 (0.41) 85 0.59 (0.29)Macrophyte Typha sp. 42 0.00 (0.00) 65 1.15 (0.40)

Triglochin procera 8 0.00 (0.00) 75 0.30 (0.15)Myriophyllum crispatum 0 ND 5 0.00 (0.00)Unidentified other 0 ND 50 0.10 (0.07)Unidentified large fibers 0 ND 25 0.00 (0.00)

Macroinvertebrate Chironomid 8 0.00 (0.00) 15 0.00 (0.00)Oligochaete 25 0.00 (0.00) 25 0.40 (0.12)Unidentified other 75 0.56 (0.32) 80 0.03 (0.03)Unidentified spine 50 0.00 (0.00) 50 0.00 (0.00)Notonectid 8 0.00 (0.00) 0 NDCherax destructor 0 ND 5 0.00 (0.00)

Other Fungi 8 0.00 (0.00) 15 0.00 (0.00)Diatoms 58 0.00 (0.00) 75 0.28 (0.10)Green filamentous algae 0 ND 15 0.00 (0.00)FPOM 83 – 95 –


ity and diet in pools with high and low ripariancanopy cover and assessing growth on differentresource types. The clear differences in resourceavailability between pools at sites with open andclosed riparian canopies were reflected in C. destructordiet. In laboratory trials, growth differed dependingon food source, a clear mechanism whereby changesin resource availability influence crayfish directly.

The influence of riparian canopy on resourceavailability was reflected in C. destructor diet. Bothallochthonous and autochthonous food sources wererepresented in C. destructor gut contents regardless ofriparian cover. However, as hypothesized, stomachsof crayfish from open sites contained a greaterproportion of autochthonous material than didstomachs of crayfish from closed sites. Similar dietaryresponses of crayfish to changes in canopy cover havebeen reported in studies of Paranephrops planifrons

from hill country streams in New Zealand (Parkyn etal. 2001) and Cambarus sp. from headwater streams inthe US (England and Rosemond 2004). However, landuse had little influence on the diets of Paranephropszealandicus in streams in New Zealand where al-lochthonous material consistently dominated crayfishdiets in both pasture and forested sites (Hollows et al.2002). However, these streams were characterized bylow amounts of instream primary production, whichmight have increased the reliance of crayfish onallochthonous resources (Thompson and Townsend2004).

Availability of different basal resources affected C.destructor resource processing and growth rates.Changes in growth rate could have importantimplications because faster growth allows crayfish to

FIG. 1. Dual stable isotope plots showing mean (61 SE)d13C and d15N signatures of Cherax destructor (from all 6sites) and potential food sources (from 1 closed and 1 opensite) from closed (A) and open (B) sites in Joyce’s Creek.Genus names are: Eucalyptus camaldulensis, Triglochin pro-cera, Potamogeton tricarinatus. CPOM = coarse particulateorganic matter.

FIG. 2. Probability distribution for inclusion of each foodsource in the diet of Cherax destructor from the closed (A)and open (B) sites based on stable isotope mixing modelresults. The maximum density for each food item indicatesthe probable proportional contribution of a food item toassimilation by C. destructor. Genus names are: Eucalyptuscamaldulensis, Triglochin procera, Potamogeton tricarinatus.CPOM = coarse particulate organic matter.


escape predation and reach sexual maturity morerapidly (Stein and Magnusson 1976, Nystrom andGraneli 1996). Cherax destructor fed macrophytematerial grew faster than C. destructor fed conditionedE. camaldulensis. This result is consistent with those ofother studies in which crayfish fed plant detritus grewslowly or not at all (Paglianti and Gherardi 2004, Rothet al. 2006) and C. destructor preferred to consumemacrophyte material over detrital food sources(Brooks 1997). Thus, loss of riparian canopy mightpositively influence C. destructor growth because areduced canopy closure was associated with in-creased cover by macrophyte and algal species andreduced CPOM standing stock. However, reductionsin CPOM standing stock could alter availability ofinvertebrate prey (Wallace et al. 1997), which wereidentified by the mixing model as an importantenergy source for C. destructor.

Crayfish diet and assimilation

Gut contents analysis in concert with stable isotopeanalysis provided a more complete picture of C.destructor ingestion and assimilation than did eithermethod alone. Mixing model results showed that E.

camaldulensis was of greater importance at the closedthan at the open site, and this result was confirmed bythe gut contents analysis. In contrast, the mixingmodel results suggested that Typha sp. contributed toC. destructor diet at the closed site, whereas filamen-tous algae contributed moderately at the open site.However, neither of these items were in highabundance in C. destructor guts. This discrepancycould have arisen if C. destructor consumed certainfoods indirectly by ingesting invertebrates that gainedC from algae and Typha sp. or by incidentalconsumption of undigested material in the guts ofprey. Food sources also might have been missing fromthe model, an issue in complex food webs that couldcontribute to false identification of C sources.

Aquatic invertebrates are important in crayfishdiets, despite the predominance of plant and detritalmatter in gut contents (Parkyn et al. 2001, Hollowset al. 2002, Beatty 2006, Olsson et al. 2008). As wefound for C. destructor, guts of P. planifrons and P.zealandicus often contain predominantly plant ordetrital matter, but stable isotope analyses indicatethat animal, rather than plant or detrital material, isassimilated (Parkyn et al. 2001, Hollows et al. 2002).Earlier studies suggested that C. destructor consumesmainly detritus and plant material (Frost 1975, Lakeand Sokol 1986). We confirmed that terrestrialdetritus and macrophyte material are more abun-dant in C. destructor guts than is macroinvertebratematerial. However, the stable isotope mixing modelshowed that C. destructor obtained more energy forgrowth from invertebrate than from plant sources,

FIG. 3. Mean (61 SE) wet mass of Eucalyptus camaldu-lensis coarse particulate organic matter (CPOM) (n = 9),Triglochin procera (n = 10), and Typha sp. (n = 10) processedover 5 d by Cherax destructor in laboratory feeding andgrowth trials. Bars with different letters are significantlydifferent (analysis of covariance with post hoc Tukey’s test;p , 0.001).

FIG. 4. Mean (61 SE) % body mass change of Cheraxdestructor fed Eucalyptus camaldulensis coarse particulateorganic matter (CPOM), Triglochin procera, Typha sp., ornothing over a period of 40 d in a laboratory feeding andgrowth experiment.


and that CPOM and biofilm contributed little ateither site. This pattern could arise from consump-tion of biofilm growing on leaves and substratebecause biofilm, like macroinvertebrates, is 13Cdepleted. However, based on the gut contentsanalysis and previous studies, invertebrates aremore likely than biofilm to be the main source ofenergy.

The discrepancy between inferences about fresh-water crayfish diet drawn from gut content and stableisotope analyses led Momot (1995) to suggest that theimportance of detritus to crayfish has been overem-phasized. Freshwater crayfish are unlikely to con-sume food sources indiscriminantly. Rather, theyprobably consume detrital and plant material inci-dentally while scavenging or hunting for macroinver-tebrate prey (Momot 1995). In food choice experi-ments, crayfish prefer to consume animal materialover detritus (Bondar et al. 2006, Roth et al. 2006). Ifcrayfish in Joyce’s Creek were feeding indiscriminate-ly, less invertebrate material would be expected thanwas observed in stomach contents because plant anddetrital matter makes up a much larger percentage ofavailable biomass than does animal material in streamsystems. Moreover, differences in biomass accumula-tion in the feeding experiment suggest that crayfishshould feed discriminately because individuals fedconditioned terrestrial CPOM had poorer growth thanindividuals fed macrophyte material. Parkyn et al.(2001) suggested that crayfish use energy obtainedfrom detritus and biofilm for respiration and mainte-nance, whereas higher quality food, such as animalmatter, contributes more to growth. Differences inquality of food sources might cause crayfish to meet Crequirements from detritus or macrophyte sourcesand N requirements from invertebrate prey (Stenrothet al. 2006).

Freshwater crayfish typically exhibit an ontogeneticshift in diet. Juveniles often consume a greaterproportion of invertebrates than do adults, and theanimal prey are thought to facilitate the faster growthrates observed in juveniles than in adults (Whitledgeand Rabeni 1997, Hollows et al. 2002, Stenroth andNystrom 2003). However, ontogenetic shifts in dietare not always observed (Bondar et al. 2005, Roth et al.2006, Bondar and Richardson 2009), and gut contentsof C. destructor from Joyce’s Creek provided noevidence of a strong ontogenetic shift in diet. JuvenileC. destructor had lower d13C values than did adults,and this result indicates a possible tendency ofjuveniles to consume additional biofilm. However,d15N values were similar between juveniles andadults, so consumption of a higher proportion ofinvertebrates by juveniles than by adults is unlikely.

Gut contents suggest that C. destructor is an omnivorethroughout its entire life cycle. However, we did notsample many juveniles and more samples might beneeded detect subtle changes in resource use withage.

Invertebrate assemblages are affected by changesin basal resources (Wallace et al. 1997, Olsson et al.2008). Thus, changes in land use that affect basalresources might influence crayfish diets directly orindirectly through their invertebrate prey. Inverte-brates made up a greater proportion of P. planifronsdiet in pasture than in forested sites (Parkyn et al.2001). In our study, the stable isotope mixing modelsuggested that C. destructor consumed a higherproportion of invertebrates in open than in closedsites. However, even closed sites on Joyce’s Creekare affected by many of the changes caused byconversion of forest to pasture (e.g., elevatednutrients, altered hydrology) because riparian forestoccurs as patches in an otherwise agriculturallandscape. Despite the influence of agricultural landuse on all sites, we detected a separate effect ofcanopy cover on crayfish trophic ecology. Thus,limited riparian vegetation has the potential toinfluence ecosystem processes even in extensivelydegraded landscapes.

The patterns we observed appear compelling, butthe study had limitations that might have influencedour results. 1) We worked in a single stream andseason, but stable isotope signatures can varyspatially and temporally. Reid et al. (2008b) foundsmall differences in stable isotope signatures amongseasons and streams in the region in which weworked and suggested that consumption of macro-phyte material might increase during summer. 2)Our study was conducted after a long drought.However, such drought conditions are becomingmore typical in southeastern Australia. 3) Moreaccurate methods for gut content analysis (e.g.,Parkyn et al. 2001) might have yielded differentconclusions, but the differences between open andclosed sites were quite large, and it seems unlikelythat our results were an artifact of the approachused. 4) The laboratory experiments providedinsights into C. destructor processing and growthwhen fed common basal resources, but a range offactors, such as intraspecific interactions, predation,food density, and microhabitat use, can affect dietunder natural conditions (Bondar et al. 2006). 5)Food sources used during feeding trials might notbe the most important sources for growth in crayfishin the field. In future studies, laboratory feedingtrials should be complemented with supplementaryfeeding in field conditions.


Implications for management

Maintaining or restoring terrestrial inputs tostreams might prevent changes to macroinvertebrateassemblages (Wallace et al. 1997, Hall et al. 2001)and crayfish resource use. Canopy cover and CPOMmass are positively correlated in lowland Australianstreams (Reid et al. 2008a, our study). Reid et al.(2008a) found that benthic CPOM mass begins toincrease at ,40% canopy cover in lowland Austra-lian streams. In our closed sites, canopy coverranged from 28 to 44%, and mass of CPOM wascomparable to that found by Reid et al. (2008a) forthis range. Thus, despite a narrow riparian vegeta-tion zone, canopy cover at the closed sites was highenough for terrestrial detritus, hypothesized to be akey basal resource in Joyce’s Creek food webs, toaccumulate in the stream. However, such a smallamount of riparian vegetation is insufficient tomaintain other structural and functional streamcharacteristics (e.g., sediment removal; Broadmea-dow and Nisbet 2004).

Assessments of the effectiveness of restorationprojects and stream health are often based onstructural characteristics of communities, such asabundance and diversity (Bain et al. 2000). However,structural measures do not provide information onecological processes, such as nutrient and energycycling, and might not reflect changes in ecosystemfunction (Harris 1994, Bunn 1995, Ryder and Miller2005). Palmer et al. (1997) suggested a focus onrestoration of community function rather than ofindividual species, and stream restoration projectsthat focus on reinstating physical habitat throughriparian management, bank stabilization, and reintro-duction of instream habitat (e.g., coarse wood) arebecoming increasingly common (Brooks and Lake2007). Information on the effects of shifts in basalresources caused by riparian loss (or restoration)contributes to our understanding of stream structureand function. In our study, changes in basal resourceavailability induced dietary shifts in the omnivorousC. destructor, and diet shifts have been observed inomnivorous fish (Zengeya and Marshall 2007). Thus,omnivores might be useful indicators of communityfunction in studies of environmental degradationinvolving basal food resources.

Our study provides important insights into thefunctional consequences of changes in resourceavailability, but work remains to be done at largerspatial and temporal scales. Our results hint atpotential indirect effects of changes in riparianvegetation on food webs as a consequence of impactson crayfish. Increased growth rate of C. destructor fed

macrophyte diets raises the possibility that riparianvegetation removal might favor crayfish in Joyce’sCreek. Faster growth rates could lead to increasedcrayfish biomass and density, which could stronglyinfluence stream food webs (Momot 1995, Nystrom etal. 1996, Brooks 1997, Peters et al. 2008). Moreover,other changes associated with riparian clearing, suchas altered nutrient and light regimes, increasedtemperatures, and soil compaction by cattle (Marchand Robson 2006), were not within the scope of ourstudy but have the potential to influence C. destructorpopulations. Thus, broader studies are needed toassess the effects of riparian loss on whole-streamfood webs, including the effects mediated by crayfishas the dominant omnivores.

Acknowledgements

Our study was done with appropriate Departmentof Sustainability and Environment collection permitsand Monash University animal ethics approval(BSCI/2008/06). We acknowledge financial supportfor this work by the Murray Darling Basin Authority.We thank Sam Lake, Susie Ho, and 2 anonymousreferees for comments on an earlier version of themanuscript, and Tom Daniel, Matthew Johnson,Andrew Fry, and Eddy Giling for field assistance,and landholders for access to Joyce’s and MiddleCreeks. Rene Diocares at Griffith University, Brisbane,did the stable isotope analysis.

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Received: 29 January 2009Accepted: 23 April 2009


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