Freshwater Btology (2001) 46, 115-160
Multi-scale effects of resource patchiness on foraging behaviour and habitat use by longnose dace, Rhinichthys cataractae
ANDREW R. THOMPSON, J. TODD PETTY and GARY D. GROSSMAN Daniel B. Warnell School of Forest Resources, University of Georp, Athens, GA 30602, USA
SUMMARY 1. We examined the response of a predatory benthic fish, the longnose dace (Rhznichfhys cataractae), to patduness in the distribution of benthic macroinvertebrates on cobbles at three hierarchical spatial scales during summer and autumn 1996, and . spring 1997 in a southern Appalachian stream. 2. At the primary scale (four to five individual cobbles separated by < 1 m), the intensity of foraging was not correlated with the biomass of benthic macroinverte- bratesi'cobble, regardless of season. 3. At the secondary scale (i.e. foraging patches < 5 m in diameter) we found that benthic macroinvertebrates were patchily distributed in summer, but not in autumn or spring. Concomitantly, in summer, longnose dace foraged on cobbles with a signifi- cantly higher biomass of benthic macronvertebrates than nearby, randomly selected cobbles with similar physical conditions (i.e. longnose dace tended to avoid low-prey foraging patches). In contrast, when benthic macroinvertebrates were distributed homo- geneously (spring and autumn), dace did not select patches with a significantly higher biomass of benthic macroinvertebrates than that available on randomly selected cob- bles. 4. At the tertiary scale (i.e. stream reaches 11- 19 m Iong), the biomass of- benthic macroinvertebrates (per cobble per reach) was patchily distributed (i.e. differed signifi- cantly among reaches) in all seasons. Among reaches with physical characteristics preferred by longnose dace, (i.e. erosional reaches dominated by cobble 'boulder sub- stratum and high current velocity), we detected a sigruficant, positive correlation be- tween the biomass of benthic macroinvertebrates,cobbleand longnose dace dens~tym all seasons. 5. Our results demonstrated that both spatial and temporal patchiness in resource availability influenced sigruficantly the use of both foraging patches and stream reaches by longnose dace.
Keywords: foraging patch, habitat selection, predator-prey, spatial heterogeneic, stream fish
Introduction Ecological systems are heterogeneous (i.e. patchy) over a range of spatial and temporal scales (Wiens, 1976,1989; Levin, 1997,; Cooper ef al., 1997).For exam- ple, habitats often contain many patch types differing Correspondence: Andrew R. Thompson, Department oi in resource availability. Resource patchiness of this Ecology, Evolution, and Marine Biology, University of California. Santa Barbara, CA 93106, USA. type may affect the behaviour of mobile species be- E-mail: [email protected] cause these individuals often occupy microhabitats
O 2001 Blackw-ell Science Ltd 145 146 A. R. Thompson et a1 that yield the highest rates of net energy intake (and, We examined the effects of spatial and temporal consequently, increase their fitness) (Fretwell & Lu- patchiness in resource availability on the toraging cas, 1971; Chamov, 1976; Cowie, 19n; Hill & Gross- behaviour, patch choice and spatial distribuhon oi a man, 1993; Morgan, Brown & Thorson, 1997). benhc stream fish (longnose dace, Ri~z>l~si~ti~uc Therefore, quantifying the effects of patchess on cataractae Valenciennes) in a temperate rood land resource use by animals should increase our under- stream. We chose longnose dace for study because it standing of how these organisms respond to environ- is an abundant species with a broad geographic range mental variation on both an individual and (Jeh& Burkhead, 1994). In the Co~veetadrainage population level (Schneider & Piatt, 1986; Hodge, (NC, U.S.A.), longnose dace are active diurnal for- 1987a.b; Orians & Wittenberger, 1991; Ward & Saltz, agers, wfuch facilitates direct obsenation of their 1994; Cooper et al., 1998). behaviour and choice of foraglng locations (A. Quantifying patchiness and its effects on animals in Thompson & G. Grossinan, pers. obsen..). Further- natural habitats can be difficult, however, for two more, longnose dace exhibit relatively high site reasons. First, patches frequently occur on several fidelity, remaining within the same stream reach hierarchical levels (i.e. larger patches contain several (14 m) for up to 18 months (Hill & Grossman, 1987). Regardless of their geographc location, adult long- smaller patches) (Urban, O'Neill & Shugart, 1987; nose dace consistently occupy riffles (i.e. erosional Kotliar & Wiens, 1990). Second, animals may not be substrata and rapid current) (Gee & Northcote, 1963; able to differentiate among patches at aU spatial Sheldon, 1968; Bartnick, 1970; Gibbons & Gee, 1977; scales (Pyke, 1981; Danell, Edenius & Lundberg, 1991; Grossman & Freeman, 1987; Hubert & Rahel, 1989; Fryxeu & Doucet, 1993). Consequently, studies of the Mullen & Burton, 1995, 1998; Grossman & Ratajczak effects of resource patmess on organisms must be 1998), where they typically prey on benthic macroin- linked to both the hierarchical distribution of patches vertebrates captured from the surfaces of larger sub- in nature and their discriminatory capabilities stratum particles (i.e. > 5 cm in diameter) (Gee & (Kotliar & Wiens, 1990). Northcote, 1963; ~erald;1966; Gibbons & Gee, 1971; Due to their high level of spatial heterogeneity Barrett, 1989; Stouder, 1990). Intraspecific competition (Pringle et al., 1988; Hildrew & Giller, 1994), temper- (mediated by food limitation), rather than interspe- ate woodland streams are model systems for address- cific competition or predation, is probably the major ing how resource patchiness affects both resource use biotic factor influencing longnose dace populations in and the distribution of animals. Based on their physi- Coweeta Creek (Stouder, 1990; Grossman et al., 1998). cal characteristics, most temperate streams can be Given the potential impact of spatial and temporal divided into several hierarchical spatial levels based patchiness in prey availability on longnose dace in on length, including: microhabitat (10-'m), riffle- the Coweeta drainage, we attempted to characterize pool (lo0 m) and reach (10' m) (Frissel et al., 1986). benthic macroinvertebrate patchiness within the svs- Patchiness in the distribution of physical factors at all tem and to quantify the subsequent responses of hierarchical levels may affect the distribution and longnose dace at three hierarchical scales during abundance of stream organisms, ranging from pri- three seasons. We measured benthic macroinverte- mary producers to tertiary consumers (Rabeni & Min- brate patchiness at primary, secondary and tertiary shall, 197;Culp, Walde & Davies, 1983; Kohler, 1984; scales following the hterarchical patch framework Parker, 1989; Pringle, 1990). In fact, both spatial and outlined by Kotliar & Wiens (1990). In this conceptu- temporal patchiness in resource availability are prob- alization, patchmess at the primary scale represents ' ably responsible for the patchy distribution of benthic the lowest level at wluch an organism can differenti- macroinvertebrates at a variety of spatial scales (Hy- ate individual patches. Scaling up, a secondary scale nes 1970; Wallace et al., 1997) including: individual patch contains at least two primary scale patches, cobbles (Muotka & Penttinen, 1994; Downes et al., whereas a tertiary scale patch encompasses multiple 1998), groups of cobbles separated by < 1 m (Dow- secondary scale patches. nes, Lake & Schreiber, 1993), and large aggregations We tested three main predictions regarding the of cobbles within stream reaches (Hynes, 1970; Dow- effects of prey patchiness on habitat use by longnose nes et al., 1993). dace. First, we predicted that patchmess in the den-
Q 2001 Blackwell Science Ltd, Freshwater Biology, 46, 145-160 Fish habitat use at rnltlfzplr scait?.; 147 sity of benthic macroinvertebrates on individual cob- (14-28 October 1996) and spring (11-19 June lW3. bles separated by < 1 m (primary scale) would result During each samphg period, we first observed fish m longnose dace foragng with sigruficantly greater by snorkelhg during daylight hours and then mea- intensity on cobbles with a hgher density of ben~c sured physical habitat characteristics and collected macroinvertebrates than cobbles with a lower den- samples of benthic macroinvertebrates. Although sity. Second, we predicted that when benthic longnose dace may forage nocturnally in Alberta macroinvertebrates were patchily distributed among streams (Culp, 1989; Scrimgeour, Culp 6r LVrona, foraging patches (i.e. cobbles separated by 0.5-5.0 m, 1994), we regularly observe longnose dace foraging the secondary scale), longnose dace would preferen- during the day at Coweeta (Grossman & Freeman, tially forage in high-prey patches (i.e. avoid low-prey 1987; Grossman & Ratajczak 1998; A. Thompson, patches). Finally, we tested the prediction that there pers. obs.). In addition, dietary studies coniirm that would be a significant positive correlation between longnose dace forage diurnally, in this system. , Iongnose dace densitylreach and mean benthic (Stouder, 1990; G. Grossman, unpublished). macroinvertebrate densityireach (i.e. sections of stream 11-19 m long, separated by distinct physical Primary scale patchiness and fhe foragirrg behnstiour breaks, the tertiary scale). of longnose dace Preliminary observations indicated that individual Methods large substratum particles (i.e. cobbles and boulders) The study site were the smallest 'patches' upon which dace foraged consistently, and we classified these particles as pri- Our study site was a 100-m segment of Ball Creek, a mary scale patches (A. Thompson & G. Grossman, fourth order stream situated on the USDA Forest pers. obs.). We will refer to these particles hereafter as Services Caweeta Hydrological Laboratory .located cobbles (i.e. unembedded particles 2 5 cm in length). within the Blue Ridge Province of the southern Ap- If patduness at the primary scale influences foraging palachian mountains. Bankside vegetation along Ball by longnose dace, we would expect a positive correla- Creek consisted primarily of rhododendron (Rhodo- tion between maaoinvertebrate density on cobbles dendron maximum L.), mountain laurel (Kalamia latifo- and the number of bites aimed at prey on cobbles by lia L.) and dogwood (Cornus florida L.). During our individual fish. We also predicted that -this relation- study, Ball Creek had a mean annual tempet.ature of ship would be strongest when macroinvertebrate 12 "C (range = 2-19 "C) and a mean wetted width of patchiness among cobbles was greatest. 5.2 m (range = 4.3-9.7 m). The major geomorphc fea- From the downstream end of the site, we tures of the site were: 1) cobble-dominated riffles; 2) a snorkelled upstream to locate actively foraging adult shallow, silty run; and 3) a sandy pool. Resident fish longnose dace ( > 45 mm standard length). Once a include mottled sculpin (Cottus bairdi Girard), long- fish was located, we counted the number of bites it nose dace (Rhinichthys catnractae) and rainbow trout took from the next four or five cobbles. We used the (Oncorhytlchus mykiss Walbaum). A weir directly be- number of bites taken by individual dace on each low the site may have blocked upstream immigration cobble (henceforth 'fish cobbles') as an estimate of of fish, although they were capable of moving down- foraging intensity. We used this metric rather than stream by traversing the weir. To facilitate spatial the time each fish spent foraging on a cobble because measurements within the site, we placed a permanent it was simpler to measure and the time increment transect pole every 4 m along both banks. between successive bites on cobbles appeared to be relatively constant (i.e. number of bites was positively correlated with the time spent on a cobble). After Sampling regime each fish completed a foraging bout, we placed a We quantified the physical characteristics of the site, unique, coloured marker adjacent to each fish cobble patchiness in the densities of benthic macroinverte- for subsequent identification. Previous research has brates and longnose dace foraging behaviour and shown that the presence of a diver does not alter habitat 'use in summer (11-21 August 1996), autumn markedly the behaviour of longnose dace in this
O 2001 Blackwell Science Ltd, Freshwater Biology, 46, 145-160 148 A. R. Thompsorz et al. system (Grossman & Freeman, 1987; Grossman & solution. We estimated the surtace area oi each fish Ratajczak, 1998; A. Thompson, pers. obs.). cobble by multiplying its maximum iength b\ it> We collected foraging data for 20 adult longnose maximum width (perpendicular tc) length). Th~s dace in each seasonal sample. This typically required method yields accurate estimates of the surtace area three sampling passes through the site. In summer, of cobbles with complex surfaces (McCreadie 6r we made three passes in a single day, but in autumn Colbo, 1991). and spring we made one pass per day on three Ln the laboratory, we identified rnacroinvertehrates consecutive days. We reduced the probability of sam- to family whenever possible. However, mites, cope- pling the same fish on more than one pass by not pods, oligochaetes, metamorphosing and pupating taking measurements if, on the second or third pass, insects and individuals with head capsule w~idths a similar-sized fish was seen within 2 m of a previ- (HCW; total distance across the head at the level of ously sampled location. After fish obsemations were the eyes) < 0.2 mm were identified only to order. We, completed, we determined the exact location of each measured HCW or maximum body width (for mites) fish cobble by triangulation with the two nearest of specimens to the nearest 0.1 mm using a dissecting transect posts on opposite banks. microscope and estimated volumes using famil!,- Because fish cobbles were in close proximity specific regression models (i.e. length-volume) de- (
C 2001 Blackwell Sc~enceLtd. Frcsliu~o!r.r Btoliyy, 46, 145-160 values would indicate high primary scale patchiness groups of fish cobbles) affected patch selection and suggest that individual longnose dace encoun- Hence, we tested for sign~hcantdlfterenceh In the tered a wide range of prey biomass/cobble. Although phvs~cal charactenshcs of foraging patch'. and CV values for macroinvertebrate biomass on goups nearby randomly selected location5 I've began th~\ of fish cobblks cannot strictly be used to estimate analyses by placmg permanent transect marker5 at quantitatively whether macroinvertebrates were 4-m mtervais along both banks of the stream (total = patchily distributed on cobbles, these values should 25 transect lmes). We then established tran5ects be useful for characterizing the degree of macroinver- across the stream (i.e. between permanent transect tebrate patchiness among groups of fish cobbles markers at the same metre mark) and collectecl ph!.s- (Palmer, Hakenkamp & Nelson-Baker, 1997). To de- ical habitat data at 1-m intervals. At each cross-stream termine whether longnose dace experienced signifi- metre mark, we placed a I-m2 grid divided into 25 cantly different levels of primary scale patchiness equal quadrats (0.04 m2 each) and then used a ran- among seasons, we compared CV values for each dom number table to select one quadrat. We seasonal sample of fish cobbles using ANOVA and quantified the physical habitat characteristics of the post hoc pairwise Tukey tests (Palmer et al., 1997). quadrat as previously described for primary scale We tested the prediction that primary scale patchi- patches. If cobbles were present, we collected ness in macroinvertebrate biomass affected the forag- macroinvertebrates from the cobble closest to the cen- ing intensity of longnose dace by testing for tre of the quadrat. We obtained physical microhabitat significant ~ correlations between macroinvertebrate measurements for 111, 116 and 118 random locations biomass,cobble and the number of bites each fish and macroinvertebrates from 87,100 and 107 random took from a fish cobble, using linear regression. If cobbles in summer, autumn and spring, respectively. primary scale prey patchiness affected the foraging As with fish cobbles, we used triangulation to locate intensity of longnose dace, then this should have the exact position of each random quadrant. produced sigruficantly more positive correlation co- To determine whether &e physical characteristics efficients then expected by chance alone. We tested of a location influenced foraging patch use by long- this prediction with a X' test (Ho: frequencies do not nose dace, we performed separate principle compo- differ significantly from a 50:50 positive:negative dis- nent analyses (PCA) on each seasonal set of physical tribution; Zar, 1996). We also tested the hypothesis data from both random locations and fish cobbles. that longnose dace would respond to primary patchi- We used the partitioned X' technique of Grossman & ness in macroinvertebrate biomass most strongly Freeman (1987) and Grossman & Ratajczak (1998) to when patchmess among fish cobbles was high. If true, test for significant differences behveen PC scores for then we would expect a positive correlation between fish cobbles and random locations. Because fish cob- the CV of macroinvertebrate biomass and values for bles were not independent (i.e. they represented correlation coefficients from correlation analyses be- groups of four to five cobbles that dace had foraged tween number of bites fish cobble and macroinverte- on), we did not treat them as independent points in brate tjiomass fish cobble. We evaluated this posji- the analysis. lnstead we calculated a mean compo- bility by performing a correlation analysis (using lin- nent score for each group of fish cobbles and com- ear regression) between CV values for macroinver- pared this score to the scores from random locat~ons. tebrate biomass, fish cobble and the correlation coeffi- We transformed data (linear-ln, percentage-arcsine cient (see Palmer et al., 1997 for discussion of the use squareroot) to reduce heteroscedast~cityand kurtosis. of CV as an independent variable). We quantified secondary scale patchiness of macroinvertebrates within the site by using spatial autocorrelation analysis to test the null hypothesis of Srcanila~/scnle patchiricss and patch use by lotigtiose no significant correlation in the macroin\.ertebrates [lace biomass values of randomly selected cobbles sepa- Our primary goal was to evaluate the effects of patch- rated by varying distances (Samelle, Kratz & Cooper, iness in prey on patch use by longnose dace. Prior to 1993; Lovvorn & Gillingham, 1996; Cooper ct al., this assessment, however, we needed to determine 1997). This analysis not only allowed the detection of whether the physical characteristics of a patch (i.e. secondary scale patches (i.e. significant correlation in
O 2001 Blackwell Science Ltd, Fresllu~aterBiology, 46, 145-160 150 A. R. Thompson et al. biomass among random cobbles), it also enabled us to riod in a portion of the drainage slightly downstre~m eshmate the size of secondary patches (maximum from our study site (Hill & Grossman, 1987). distance between sigruficantly correlated cobbles). We estimated iongnose dace densiv in each reach Using the X-Y coordinates of each random cobble, by dividing the number of longnose dace obsen-ed (n we calculated the distance between cobbles to the a reach by its area. We minimized the prohabill? that nearest 0.05 m. We then calculated Pearson's product- individual longnose dace were counted repeatedl! b\. moment correlation coefficients (r) for biomass values deleting individuals of similar size observed within of pairs of cobbles separated by 0-1, 1-2, 2-3 and 2 m of a previously identified fish. Nonetheless, thi5 3-5.4 m along transect lines. We chose these dis- only resulted in the elimination of a small number of tances because we observed that longnose dace never fish (0 in summer, 1 in autumn and 1 in spring). In moved more than 5 m during a forapg bout (A. order to validate visual estimates of fish density, we Thompson and G. Grossman, pers. observ.). Finally, electrofished each reach after all samples had been we created a correlelogram for each seasonal data set collected in spring (we did not electrofish.in other by plotting correlation coefficients (Y) versus distance seasons to avoid disturbing fish). Visual obsemahons class (X) for all pairs of random cobbles. To avoid of fish number were either exactly the same (reaches violating the assumption of independence, cobbles 1-4) or differed by one (reach 7) or two (reach 6)hsh were used once only for each distance class analysis from electrofishing estimates. In reach -5, hon.ei.rr. (Underwood & Chapman, 1996). electrofishmg accounted for five iish, \\.hlle We tested the null hypothesis that secondary scale snorkelling observations failed to identity any iish patcbess had no effect on foraging patch use by This discrepancy was caused either by post- longnose dace by ascertaining whether macroinverte- snorkelling fish movement or our inability to obser\,t. brate biomass on fish cobbles (i.e. in foraging patches) fish accurately in reach 5. We believe that the latter differed significantly from that on random cobbles explanation is not entirely correct because we ob- with similar physical characteristics. For each fish, we served longnose dace in reach 5 in summer and chose the nearest random cobble that was > I m autumn. Consequently, some longnose dace probablv from its foraging patch. Because our results indicated moved into reach 5 following disturbances associated that longnose dace in Coweeta Creek avoid deposi- with data collection. In spite of the incongruity asso- tional areas, we chose only random cobbles found in ciated with reach 5, linear regression indicated that erosional locations. As with the physical data, we did visual estimates of dace abundance reach were hghlg not treat individual fish cobbles as independent correlated with estimates derived from electrofishing points, but calculated an average macroinvertebrate (r = 0.76, P = 0.04, d.f. = 6),suggesting that visual ob- biomass value for each fish from the four to five servations were effective at determining dace abun- cobbles in a foragmg patch. *we then used a paired dance with the site. t-test to. test for significant differences between the If tertiary scale (i.e. among reach) patchiness In fish and random data sets. macroinvertebrate biomass affected the distribution of 'longnose dace, then we would expect a s~bmificant positive correlation between the biomass of macroln- Tertiary scale patchiness and longnose dace vertebrates and abundance of longnose dace across abundatlce reaches. However, given that adult longnose dace are We examined the distribution of longnose dace at the often under-represented in depositional microhabi- tertiary scale by dividing the site into seven reaches tats (Grossman & Freeman, 1987; Grossman & Rata- bounded by either natural barriers (i.e. where > 70% jczak, 1998), physical differences among reaches may flow was diverted) or distinct geomorphological have also affected distribution patterns. Conse- changes (e.g. shifts from pool to riffle). Mean reach quently, we first assessed whether the physical char- length (i.e. tertiary patch) was 12 m (range = ll- acteristics of reaches differed and whether these 19 m) and mean reach area was 81 m' (range = 51- differences were correlated (using linear regression) 133m2). The length of tertiary patches also with dace density. Second, we quantified patchiness corresponded to mean home range size of longnose in macroinvertebrate biomass among reaches (see be- dace, which averaged 13.4 m over an l&month pe- low) and then tested the prediction that reaches phys-
O 2001 Blackwell Science Ltd, Freshwater B~ology,46, 145-160 Fish habitat usc at multrplc sa7lt.s 151 ically suitable for dace would also display a sigrufi- iness in macroinvertebrate densities on fish cobbles ~n cant positive correlation (using hear regression) be- any season. First, the frequency oi positi.i.e correiat~nn tween macroinvertebrates biomass and the coefficients between macroinvertebrate biomass and abundance of longnose dace. foraging intensity (i.e. the number of bites taken) by To quanhfy thud order patduness in the physical individual fish did not differ from that expected by environment, we tested the hypothesis that mean chance alone (number of fish displaying positive r's principal component 1 (PC 1) scores generated sepa- in summer = 8/20, autumn = 9 30, spring = 10 110, all rately for each seasonal data set (see above) differed X' P's > 0.10). Second, the CV of macro~n~ertebrate sigruficantly among reaches. We were unable to meet biomass was not correlated with the correlation co- normality assumptions necessary for standard para- efficient between macroinvertebrate biomass and for- metric analysis, so we utilized Kruskal-Wallis analy- apg intensity (summer r = 0.21, autumn r = 0.113, sis to test for overall differences and an a posteriori spring r = 0.20, all P's > 0.10). These results suggest Nemenyi test (Zar, 1996) to evaluate painvise differ- that patchiness in macroinvertebrate biomass among ences. Once the physical nature of each reach was fish cobbles (i.e. primary scale patchmess) had little identified, we used X' analysis to test the hypothesis impact on the foraging behaviour of longnose dace: that longnose dace abundances in depositional reaches were lower than those expected by chance Secondary scale patchiness and patclr irse by lor~gnose alone (Zar, 1996). dace We quantified third order patchiness by testing the Principal component analysis and partitioned X' tests hypothesis that mean macroinvertebrate biomass demonstrated that the physical characteristics of varied si,pificantly among reaches. As with physical patches significantly affected foraging patch use by data, we were unable to meet normality assumptions longnose dace in all seasons. Principal component and, consequently, utilized a Kruskal- Wallis analysis analysis extracted three to four components with ei- to test for overall differences, followed by a Nemenyi genvalues greater than 1 from each seasonal set of test of painvise differences (Zar, 1996). Using linear habitat availability data. However, we retained onls regression, we tested the null hypothesis of no sigrufi- PC 1 because it explained the greatest amount of total cant correlation between macroinvertebrate biomass variance within the data (26% in summer, 32"b in and fish abundance among reaches using regression autumn and 31% in spring), and also depicted the analysis. Because longnose dace apparently avoided major habitat gradient (erosional-depositional) depositional reaches irrespective of food availability present in the site. Partitioned X' analyses demon- (see Results), we restricted the regression analyses to strated that longnose dace were significantly under- erosional reaches. All statistical calculations were represented in patches with low velocity and made using Microsoft Excel and SAS (SAS Institute, depositional substrata in all seasons (summer X' = Cary, NC). 15.4 P = 0.008, autumn X' = 0.026 P = 0.026, spring x2 = 15.3 P = 0.018, Fig. I). Results The presence of secondary scale patchiness in the biomass of macroinvertebrates varied among seasons. Primary scale pafdriness anti the foragirlg beharioltr In summer, macroinvertebrate biomass was posi- of longnose dace tively correlated for cobbles within 3 m of each other- Primary scale patchiness in the biomass of macro- (Fig. ?-). In autumn and spring, however, we failed to invertebrates within foragmg patches varied among detect significant autocorrelation at any distance class seasons. Summer coefficients of variation (CV) for (Fig. 2). macroinvertebrate biomass on fish cobbles (0.48 When secondary scale patchiness .in macroinverte- 0.05, mean i SE) were significantly lower than values brate density was present (i.e. summer), longnose for both autumn (0.94 0.09) and spring (0.78 = 0.06) dace foraged in patches with significantly greater (F = 10.9, P < 0.001, d.f. = 59). ~es~iiehigh CV values macroinvertebrate biomass than that observed on for macroinvertebrate biomass in autumn and spring, random cobbles with similar physical characteristics there was no evidence that the foraging intensity of (Table I). Ln contrast, when secondary scale patchi- longnose dace was influenced by primary scale patch- ness in macroinvertebrate biomass was not observed
@ 2001 Blackwell Science Ltd, Freshwatm Biology, 46, 145-160 152 A. R. Thonzpson et al.
0 25 Random kuturnq n=116 020 C w Z 015. a, ; 3 i; ;;; g 010 005 1 LL 005. 0 00 ,mmer 38 33 28 23 ,18 13480303 08 13 18 23 0 00 dl -3 8-3 3-2 8-23-1 8-13-0 8 0 3 0 $ 0 8 1 3 1 E 2 :: % Cobble (0 73) Oh Silt (-0 72) Ave current veioc~ty(0 72) Oh Debris (-O 58) % Cobble ( 70) Bottom current velocity (0 69) % Stlt (-0 57) Ave current veloc~ty1 88) i 2 % Debris (-0 52) BoRorn current velocity ( 85)
Fish i 2 05, ""20 040 - I 0 35 - ;i;h20 04 2, 0 30 0 5 03 $ 025
cr 2 020 J z024 w9 0.15 - U, I 0.1 - 0.10 + 005 -
0 0 -3 8-33-2 8-2 3-1 8-1 3-08-0 3 0 3 0 8 1 3 1 8 2 3 -38-33-28-23-18-1348-030308 13 18 23 0 00 I
(a) Principle Component 1 (b) Principle Component(II 1 Random Spr~ng 030 n=118 I 025 i I g 020 * w $ 015. 2 lL010 0 05
0 00 --I II I
Oh Cobble (0 80) O/O Sand (-0 43) Ave current velocity (0 80) YO S~lt(-0 71) Bottom current veloc~ty(0 80) % Gravel (0 4 1 )
-38.3 3-2 8.2 3-1 8.1 3-0 8.0 3 0 3 0 8 1 3 1 8 2 3 (c) Principle Component 1
Fig. 1 Patch use on PC 1 in summer (a), autumn (b) and spring (c). Histograms represent frequency d~stributionsof PC 1 scores for random and fish locations. Variables with component loadtngs > jO.4, are I~sted.
O 2001 BIackwell Sclence Ltd, Freshu~att~Biology, 46, 145-160 Fish habitat use at nlult~ple~iillt'~ 153
Summer 10 -,,-;: 08. Summer ?.I .-.. - -1 .O -0.5 0:O 0 5 ! 0 o,b cobble r O :? i 96 Silt (-0.71'1 ale. vel (0.-21 % Drbns (-0.58'1 honom ,0 09,
Autumn 10 14 7613 C as! Autumn j ...... 06 - -1.0 -0.5 0 0 0.5 i u 40 Cobble (0'0) % S~lt(-0.57) a~ebe1 (0 88) 76 Debns (-0 52) bonom vel (0 83, P Spnnf 6'135 . .. me. - COCobble (0.80) 96 Sand (-0.43) Ave vel. 10.85) % Silt (-0.71) Bonorn vel. (0 XOi ?/o Gravel (0.4l < - -
Fig. 3 Mean PC 1 xore per reach in summer. autumn and spring. Horizontal bars depict reaches that did not difter based on a Nemenyi test. Reaches are identified bv the numbers above the symbols. Only variables with component loadings > 10.41 are listed.
Fig. 2 Correlogram of benthic macroinvertebrate biomass in sons (Kruskal-Wallis tests on PC 1 xores - summer summer, autumn and spring. Distance class represents the x2 = 31.4 P < 0.01, autumn x2 = 22.3 P < 0.001, spring range of distances separating pairs of cobbles. Significant x2 = 36.1 P < 0.001, Fig. 3). These analyses indicated regressions (P c 0.05) are depicted by *. that the site was comprised of two significantly dif- (autumn and spring, Fig. 2), there were no significant ferent groups of reaches (erosional reaches with high differences in he biomass of macroinvertebrates be current velocity and cobble-dowated substratum tween paired fish and random cobbles (Table 1). [reaches 2, 3, 5, 6 and 71; and deposltlonal reaches with a low current velocity, sand, slit and debris- dominated substratum [reaches I and 41). Tertiay,scale patchiness and fhe abundance of Chi-square tests indicated that significantly fewer longnose dace longnose dace were found in the depositional reaches Reaches within the study site displayed tertiary scale (1 and 4) in each season than was expected by chance patchiness in physical characteristics during all sea- alone (summer P 0.025, autumn P < 0.10 and sprlng
Table 1 Pair-wise comparisons of macroinvertebrate biomass (pL cm-2) and PC 1 scores between foraged-upon (n = 70) and random cobbles (n = 20). Only random cobbles with similar PC 1 xores to fish cobbles were selected for the analys~s
Macroinvertebrate Macroinvertebrate PC 1 score fish PC 1 score random Season biomass fish cobbles (ZSE) biomass random cobbles (EE) t P cobbles (2SE) cobbles (2SE) t P
Summer 0.28 (0.03) 0.20 (0.07) 2.05 0.03 0.61 (0.17) 0.57 (0.17) 0.40 0.35 Autumn 0.23 (0.07) 0.21 (0.09) 0.28 0.39 0.69 (0.17) 0.63 (0.18) 0.55 0.39 Spring . 0.32 (0.10) 0.26 (0.11) 0.78 0.22 0.55 (0.10) 0.63 (0.17) 0.83 U 11
O 2001 Blackwell Science Ltd, Freshwater Biology, 46, 145-160 154 A. R. Thompson et al. lJ < 0.035). In summer and spring, no- fish were ob- Discussion served in reaches 1 or 4, while m autumn one fish The capability of many animals to select toragin;: 4. was observed in reach locations that maximize their rate of energy gain Tertiary scale patchiness in the biomass of macro- (Chamov, 1976; Hill & Grossman, 1993; llor,LTan c7t i~j., invertebrates was present in all seasons (Kruskal- 1997) is dependent upon an abilic to reco,mize and Wallis test all P's < 0.01). In summer, Nemenyl - to evaluate resource patches over a range of spatla1 tests demonstrated that reaches 1, 2, 3 and 5 had scales (Schmidt & Brown, 1996). h'e tound that re- sigruficantly higher macroinvertebrate biomass than source patchiness (i.e. spatial variation in resource reaches 4 or 7 (Fig. 4). In addition, reach 2 also had availability) significantly affected the distribution of significantly higher macroinvertebrate biomass than longnose dace both within and among reaches. The reach 6 (Fig. 4). In autumn, reaches 1 and 2 had presence and magnitude of this response, however, significantly higher macroinvertebrate biomass than was strongly influenced by spatial and temporal reaches 4 and 6 (Fig. 4). Finally, in spring, reaches 1, patchiness in resource availability during the course 2 and 3 had significantly higher macroinvertebrate of our study. At the primary spatial scale (i.e. individ- biomass than reaches 4 and 7 (Fig. 4). ual cobbles), we detected no relationship between Tertiary scale patchiness in macroinvertebrate macroinvertebrate biomass and the foraging intensity biomass influenced the spatial distribution of long- of longnose dace in any season. At the secondary nose dace across reaches. There were strong positive scale (i.e. foraging patches within reaches), when correlations between macroinvertebrate biomass and longnose dace density within erosional reaches in macroinvertebrates were patchily distributed within the site (i.e. summer), longnose dace preferentially every season (summer r = 0.98 P = 0.003, autumn r = occupied patches with significantly higher prey 0.96 P = 0.008 and spring r = 0.86 P = 0.059, Fig. 5). biomass. In contrast, this result was not obtained when macroinvertebrates were not patchily dis- tributed (i.e. autumn and spring). Finally, we de- tected tertiary scale patchiness (i.e. among reaches) in
A Summer the biomass of macroinvertebrates in all seasons, and 0.25 ; longnose dace densities were consistently correlated with hspatchiness. 0.15 . Given that both secondary and tertiary scale patch- 0.10 . iness in the biomass of macroinvertebrates signifi- 0.05 * cantly influenced patch choice and the spatial 0.00 - 0 25 A Autumn distribution of longnose dace, we were surprised that hl longnose dace did not respond to prey patchiness at g 020 the primary scale. Our findings are not unique, how- ever, for Ives, Kareiva & Perry (1993) also found that predatory lady beetles, Coccinella 7-punctata Linnaeus 005 m0 and Ifippodamia variegata Goeze, responded to patchi- 0 00 ness of their aphid prey Macrosiphum euphorbiae 0.40 A 0.35 . Spring Thomas at secondary (individual plants) and tertiary 0.30 (groups of plants) scales but not at the primary scale (individual leaves). In addition, Fryxell & Doucet 0.15 . (1993) found that beaver, Castor canadensis Kuhl, ac- 0.10 0.05 tively selected high-quality sapling stands but, once 0.00 with a stand, did not differentiate among individ- 1234567 Reach ual saplings. One potential explanation for these find- ings is that the behaviour of individuals in complex Fig. 4 Mean macroinvertebrate biomass per reach in summer, autu.mn and spring. Letters depict reaches that differed environments may be highly variable over short peri- s~gnihcantlybased on a Nemenyi test (P < 0.05). ods of time (Gray, 1987), and that short-term sam-
O 2001 Blackwell Science Ltd, Freshwater Biology, 46, 145- 160 Flsh Izabitat use at nll~ltiplcsia1t.s 153
pling simpiy is incapable of detecting the.subtle re- In contrast to macroinvertebrate patchmess at the sponses of some animals to patduness at the primary secondary scale, we detected patchiness in the den- scale. Our futdings, as well as those of Ives et al. sity of macroinvertebrates at the tertia~(i.e. reach) (1993) and Fryxell & Doucet (1993), suggest that re- scale in all seasons. Furthermore, tertiary scaie patch- sponses to environmental patcluness by animals may iness in prey distributions explained the vast majority often not be evident unless examined at multiple of variance in dace abundance among reaches (i.e. spatial scales. 74-96%). Therefore, although longnose dace did not The ability of animals to forage in patches with choose foraging patches with high prey biomass in all high prey density can be influenced strongly by the seasons, they did preferentially occupy reaches with level of patchiness present in the local environment. high prey biomass throughout the study. In environments where patch boundaries are vague, Tertiary scale (reach scale) patchiness in benthic animals are less likely to forage in locations of high macroinvertebrate biomass has been detected in tem- prey (Gilinsky, 1984; Tokeshi & Pinder, 1985; Kareiva, perate streams other than Ball Creek (Downes et al., 1987; Tokeshi, 1994; Schmidt & Brown, 1996). For 1993). Working in an Australian stream, Downes e! example, Grand & Grant (1994) found that convict al., (1993) found that benthic macroinvertebrate den- cichlids, Cichlasoma nigrofasciatum Guenther, do not sity differed sigruficantly between adjacent riffles. forage consistently in patches with hgh prey They cautioned investigators against assuming availability when the spatial distribution of prey is reaches are homogenous based on physical character- unpredictable. However, when the location of prey istics because the biotic environment can be highly patches is predictable, convict cichlids typically for- variable. Our results reinforce this cmeat, as do the age in lugh-prey patches (Grand & Grant, 1994). Sirn- findings of Grossman, Hill and Petty (1995). ilarly, the failure of Iongnose dace to choose more Although food 'availability was undoubtedly an profitable foraging patches in autumn and spring important factor influencing habitat-use patterns of may have been affected by a lack of clear patch longnose dace, the physical characteristics of habitat boundaries (i.e. no significant prey patchiness) in the patches also affected habitat use by this species at site during these seasons. several spatial scales. Our results indicated that long- Our finding of seasonal variation in secondary nose dace consistently avoided both depositional (i.e. scale patchiness in macroinvertebrates may be related low current velocity, high amounts of sand, silt and to seasonal variation in the availability of benthic debris) patches and reaches. If the phy;ical character- organic matter in this system. The macroinvertebrate istics of a reach did not provide adequate habitat for - assemblage in the Coweeta Creek drainage is domi- longnose dace, it was not used even if food was nated by detritivores (collector-gatherers and shred- abundant. For example, although reach 1 (a deposi- ders), whose distribution and abundance are strongly tional reach) had high mean benthic macroinverte- affected by seasonal variations in resource availability brate density in all seasons (Fig. 3), we failed to (Wallace, Webster & Meyer, 1995). In autumn, when observe a single adult longnose dace in ths reach leaf litter is ubiquitous, detritus tends to be more during our study. Similarly, Wallace et al. (1995) uniformly distributed in southern Appalachian found that habitat use by stream macroinvertebrates streams than in oilier seasons (J. Hutchens, unpub- could be constrained by abiotic factors even when lished data). After leaf fall, however, hgh flow events food levels were high. and decomposition tend to produce aggregations of Our conclusion that adult longnose dace avoided detritus (i.e. patches) (Webster et al., 1994). Therefore, depositional habitats is consistent with other studies as the year progresses from autumn to late summer, (Hubert & Rahel, 1989; Mullen & Burton, 1995, 1998). it is likely that the distribution of detritus becomes For example, Grossman & Freeman (1987) and Gross- less homogeneous and increasingly patchv in the man & Ratajczak (1998) found that adult longnose Coweeta drainage. Because collector-gatherer distri- dace (i.e. > 5 cm SL) occupied habitats with high butions are strongly affected by food availability current velocity and erosional substrata. In addition, (Culp ef al., 1983), it follows that both detritus patches longnose dace from streams in Alberta and British and patches of benthic macroinvertebrates would be Columbia, Canada also occupied riffle habitats with most discrete in late summer (Webster et al., 1993). lugh current velocities (Gee & Northcote, 1963; Cib-
O 2001 Blackwell Science Ltd, Freshwater Biology, 46, 115-160 156 , A. R. Tizon~psonet al. prey availability on habitat use bs stream iish, hot\.- '* summer '2 ever, may lead to erroneous results. For example, 0.10 / ' Fraser & Sise (1980) attempted to predict the abun- dance of blacknose dace (Rhi~ziclrtl~usotri7tlrlus Her- mann) among stream reaches based on the physical characteristics of these reaches. The!, hypothesized that reaches with high-qualit). ph!.sical characteristics also would have a hgh food level and, consequently, high blacknose dace density. However, the model of 0.07 - Fraser & Sise (1980) failed to predict accurately the N : Autumn E 0.06 , abundance of blacknose dace among reaches, a result they attributed to an' insufficiently precise habitat quality rating system. Had we attempted to use the availability of cobble-riffle habitat within reaqhes to predict longnose dace abundance, our results would also have been probIematica1. For example, reach 6 had adequate physical characteristics (i.e. high cur- 004 008 012 016 020 0 08 Spring rent velocity, erosional substrata), but relatively low prey density. Therefore, in terms of physical condi- 006 - tions, reach 6 could be classified as a 'high-qualit>. tertiary scale patch', whereas in terms of prey den- sity, it represented a 'low-quality tertiary scale patch'. Low-prey density in reach 6 probably accounted for 0.02 - 1 the low abundance of Iongnose dace in th~sreach (Fig. 5). 0 00 4 0 1 0.2 0.3 0.4 The identification of tertiary scale patches that had Macroinvertebrate Biomass (yl cm-*) adequate physical characteristics for longnose dace, but inadequate biological resources, has important Fig. 5 Regression of mean macroinvertebrate biomass and implications both for fish conservation and manage- longnose dace density in summer, autumn and spring including best-fit regression line. Data are presented only for ment. A common finding in studies of fish-habitat erosional reaches. Reach numbers are represented next to relationshps is that, although fish abundance is con- each symbol. sistently low in habitats with inadequate physical conditions, the abundance of fish in areas with appar- bons & Gee, 1972). Furthermore, Sheldon (1968) ently suitable physiognomy varies substantially found that longnose dace were obligate riffle dwellers (Fausch et al. 1988). Tenell et al. (1996) termed this in a thud order stream in New York. relationship a 'wedge-shaped curve'. A likely expla- Our general findings also underscore the impor- nation for the high variability in fish abundance in tance of quantifying the effects of both physical and locations with suitable physical habitat characteristics biological resources on habitat use in stream fish. is that prey abundance also varies considerably Although many investigators have examined the rela- among these locations. It is possible 'that the inclusion tionship between physical habitat characteristics and of prey abundance in models of habitat suitability' habitat use,abundance of stream fish (Gonnan & will greatly increase our ability to predict fish abun- Karr, 1978; Ross, 1986; Grossman & Freeman, 1987; dance with reaches of a stream. Fausch, Hawkes & Parsons, 1988; Gorman, 1988; Our study is one of the first to address how patch- Greenberg, 1991; Grossman et al., 1998), fewer studies iness in both physical and biological habitat charac- have examined habitat use or abundance of stream teristics at multiple spatial scales affected the fish in relation to prey distributions (Fausch, 1984; behavior, patch choice and spatial distribution of a Hughes & Dill, 1990; Hill & Grossman, 1993; Petty & common stream fish. Longnose dace in the Coweeta Grossman, 1996). Failure to quantify the effects of drainage responded to resource patchiness at both
O 2001 Blackwell Science Ltd, Freshwater Biology, 46, 145-160 Fish lrahitat rise at nrultiple scalci 157 secondary and tertia~scales, but failed to respond at Cooper S.D., Bamuta L., Samelle O., Kratz K. 6- the primary scale. These results suggest that a hierar- Diehl S. (1997) Quantieing spatial heterogeneity in chical approach to habitat use and environmental streams. Iourtlnl qf tkt. Nortlr Anlcricnt~ EctrtIlr~lclyr;,;i patchiness will increase our understanding of how Society, 16, 174- 188. organisms respond to their environment. Cooper S.D., Diehl S., Kratz K. & Samelle 0. (199s) Implications of scale for patterns and process in stream ecology. Austrnlian Journnl oi E~olc)~y,23, Acknowledgments 27-40. We gratefully acknowledge the help of the following Cowie R.J. (1977) Optimal foraging in great tits (Parus people with field work: M. Farr, J. Little, K. McDaniel, mqiOr). Nature, 268, 137-139. R. Ratajczak, A. Schroeer and L. Shuff. M. Freeman, Culp J.M. (1989) Nocturnally constrained foraging of M. Hunter, C. Osenberg and J. Wallace helped de- a lotic minnow (Rhinichthys catamctae). Canadintr velop and formalize many of the ideas presented in Iou~zQ~of ZOO~O~Y,67, 2008-2012. this study. The manuscript was improved by the Culp J.M., Walde S.J. & Davies R.W. (1983) ~elatille comments of C. Gibson, M. Hunter, M. Fan, K. Mc- importance of substrate particle size and detritus to Daniel, C. Osenberg, B. Ratajczak, J.B. Wallace and stream benthic macroinvertebrate microdistribu- two anonymous reviewers. In addition, we would tion. Canadian Journal Fisheries and Aqunfic Scirncc, like to acknowledge the years of guidance, logistical 40, 1568-1574. support, and access to the site provided by 0. KIoep- Danell K., Edenius L. & Lundberg P., (1991) Her- pel, W. Swank, L. Swift, B. Cunningham and the staff bivory and tree stand composition: moose patch of the U.S.Forest Service Coweeta Hydrologic Labo- use in winter. Ecology, 72, 1350-1357. ratory. Financial support for this project was pro- Downes B.J., Lake P.S. & Schreiber E.S.C. (1993) Spa- vided by grants from the U.S. Department of tial variation in the distribution of stream inverte- Agriculture McIntire-Stennis program (grant nos. brates: implications of patchiness for models of GEO-0037-MS and CEO-0086-MS), the National Sci- community organization. . Freshwater Biology, 30, ence Foundation (BSR-9011661), the Daniel B. Wamell 119-132. School of Forest Resources, and the University of Downes B.J., Lake P.S., Schreiber E.S.G. & Slaister A. Georgia. (1998) Habitat structure and regulation of local spe- cies diversity in a stony, upland stream. Ecological Monogmplrs, 68, 237-257. References Fausch K.D. (1984) Profitable stream positions for Barrett J.C. (1989) Tke efecfs of cornpetifion and resource salmonids: relating specific growth rate to net en- nzailahility on the belrnzlior, microhabitat use, and diet of ergy gain. Canadian ]ournal of Zoology, 62, 441-451. tlte ntottlcd sctilpbr (Cotttts bnirdi). Ph.D. Dissertation, Fausch K.D., Hawkes C.L. & Parsons M.G. (1988) Uni\,ersity of Georgia, Athens, GA. Models that predict standing crop of stream fish Bartnick V.G. (1970) Reprdductive isolation between from habitat variables: 1950-1985. In: Geil Tech Rep two sympatric dace, R~~znickthysntrat~rlus and R. PNW-GTR-213. Department of Agriculture, Forest catnractne, in ~anitoba.jourt~al of the Fiskeries Re- Service, Pacific Northwest Research Station.. smrclt Bonrd Cannda, 27, 2125-2141. Fraser D.F. & Sise T.E. (1980) Obsewations on stream Bovee K.D. & Milhous R.T. (1978) Hydraulic simula- minnows in a patchy environment: a 'test of a the- tion in instream flow studies: theory and technique. ory of habitat distribution. Ecology, 61, 790-797. In: Instrcnm Floul Pnper No. 5. U.S. Fish and Wildlife Fretwell S.D. & Lucas H.L. (1971) On territorial be- Service,Office of Biological Services 78,33. havior and other factors influencing habitat distri- Chamov E.L. (1976) Optimal foraging, the marginal bution in birds. I. Theoretical development. Acta value theorem. ~~leoretica~Population Biology, 9, Biotheoretica, 19, 16-36. 129-136. Frissel C.A., Liss W.J., Warren C.E. & Hurley M.D. Ciborowski J.J.H. (1983) A simple volumetric instru- (1986) A hierarchical framework for stream habitat ment to estimate biomass of fluid-preserved inver- classification: viewing streams in a watershed con- tebraks. Carraiiinrr Etrtonlologist, 115, 427-430. text. Envirottmental Management, 10, 199-214.
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