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Behaviors Responses of Drunelh coloradensis Ephemeroptera Nymphs to Short-Term pH Reductions

Christopher M. Pennuto and Frank deNoyelles, Jr. Department of Systematics and Ecology, University of Kansas, Lawrence! KS 6604.5-2 7 06, USA

Pennuto, C.M., and F. deNoyebles, Jr. 1993, Behavioral responses of Drupsella coloradensis (Epherneroptera) nymphs to short-term pH reductions. Can. 1. Fish. Aquat. Sci. 50: 2692-2697. Behavioral responses of Drunelba cs/oradensis nymphs were examined in outdoor experimental stream channels aker pH reductions of 7 and 2 pH units below ambient. The severity of pH decline below the ambient of 7.8 influenced the behavior patterns displayed by nymphs. At pH 7.01 (an intermediate pH decline) nymphs sat less frequently and burrowed more than controls. Burrowing behavior frequency returned to control levels and drifting and crawling behaviors increased relative to controls at pH 6.02, Ventilatory behaviors increased with pH decline, but were independent of the severity of acidity increases. These results suggest that individual behaviors may offer a more sensitive indicator of sub-acute stress in aquatic communities than population or community monitoring. Behaviors leading to increased activity levels in stream may have community-level effects via changes in predator-prey encounter rates or increased susceptibility to passive drift. These potential changes are discussed in reference to monitoring for acidification effects.

On a 6tudi6 les comportements de nymphes de Druneh cobradensis dans des tronCons de cours d'eau exp6rirnentaux aprPs une r6duction de I et 2 unites de pH par rapport au pH ambiant. La gravit6 de la baisse de pH par rapport au pH arnbiant de 73, a influenc6 les comportements manifest& par les nymphes. A pH 7,01 (soit une baisse intermediaire du pH), les nymphes se posaient rnoins fr6quemrnent et s'enfouissaient davantage que ies temoins. La fr6quence du comportement d'enfouissernent retrouvait celle des groupes-tkrnoins et les comportements de dkrive et de rampement se faisaient plus fr6quents par rapport aux temoins, 21 pH &,02. Les comportements ventilatoires se sont accrus ii mesure que le pH baissait, mais ils 6taient independants de la gravite de ['acidification. Ces resultats donnent 5 penser que les comportements individuels peuvent csnstituer un indicateur plus sensible du stress subaigii dans des communaut6s d'insectes aquatiques que ne l'est la surveillance des populations ou des communaut6s. Des comportements qui conduisent ii une activit6 accrue chez les insectes lotiques peuvent avoir des effets au niveau de la cornmunaute dans la mesure oG sont modifi6s les taux de rencontre entre predateurs et proies ou encore est accrue la susceptibilit6 2 une derive passive. (I est question de ces changements en termes de surveillance des effets de I'acidiiication.

Received April 7, 1993 Rep 1e 7 a vril 1993 Accepted luly 9, 1993 Accept4 le 9 juilBet d 993 (JB878)

.ic ecologists have demonstrated that reduced pH and environmental) might also act to increase or decrease the A:; and have negative effects on individuals, populations, likelihood of drift and no research demonstrates whether other communities of aquatic insects. To assess the behaviors in insects are altered under acid stress (but McCahon potential impacts of acidification in lotic systems, researchers et al. (1989) have addressed changes in feeding rates of have monitored colmgmity level effects on benthic density, amphipods and snails in relation to increased acidity). The diversity, or functional group abundance (Fiberg et al. 1980; importance of insect behaviors in response to acidification and Hal1 et al. 1980; Hildrew et al. 1984; Pallard and Moreau 1987; the implications of behavioral alterations in determining the Hopkins et al. 1989; Hall 1990). Studies concerning individual outcome of higher level interactions has not yet been addressed. responses to acidification have focused on physiology, body Aquatic insects might use behaviors such as drifting or mass changes, and survival or emergence (Bell 1971; Fiance burrowing to evade exposure to short-tern1 increases in acidity 1978; Mavas and Hutchinson 1983; Allad and Msreau 1986; One might expect some behaviors to predominate depending on Cornea et al. 1986; Hemann and Andersson 1986; Wowe et al. the severity of the disturbance (Resh et al. 1988) and the 1988, 1989; Mackie 1989; Chmielewski and Hdl 1992). Drift energetic trade-offs between behavior and physiology (Dill rates are probably the most widely examined response to 1987). In particuIar, regulatory behaviors (e.g., Wiley and Kohler acidification (Hall et al. 1980; Pratt and Hdl 1981; Bmerod 1984) often involve conflicts with other behaviors md we likely et al. 1987; Hopkns et al. 1989; Bernard et al. 1990): generally to be the most sensitive indicators sf stress. For example, under drift increases in most taxa. Grazing (e.g., baetids and low oxygen conditions metabolic carbon dioxide must be siphlonurids), and small chironomid midges (Orthcladiinae) counteracted before tissue acidosis occurs (Nation 1985). appear to be the most sensitive insects to reduced pH. Although Mayflies might increase gill ventilation rates to overcome a increased drift rates have been documented with experimental minimal oxygen debt or drift if the oxygen stress is severe acid additions, it is unknown whether this drift response is active, (Eriksen 1963; Wiley and Kohler 1988). Drifting, howeven; may passive, or a combination of these. Other factors (both genetic pose added predation risks from visually feeding fish (Waters

2692 Can. 9. Fish. Aguat. Sci., \Gl. 50, 1993 1972; Allan 1978, 1984; Stewart and Szcytko 1983; Skinner TABLE1. Water chemistry for the Mullem Creek (MC) shady site and 1985). Thus, a conflict would arise if predation risk was high and Little Brooklyn Lake inlet (EB) nymph collection site on 8 August 1991. oxygen stress was greater than could be overcome by increases All measurements are in ~eqLunless stated otherwise. in ventilation rate. site As with a low oxygen stress, increased acidity may lead to a physiological disruption that requires rectification. In mayflies, metabolic ion concentrations are disrupted with increasing acidity (Rowe et a%.1988, 1989; but see Bemill et al. 1991), and pH depending on the costs, certain behavioral responses might be Ternperatua-e ("C) Conductivity (y~/crn~ expected as counter measures. For example, behaviors which Alkalinity ensure adequate evasion of the stress, yet do not increase ca2+ predation risks, might be favored. If behavioral responses to kIg2+ stress maximize regulatory efficiency based on energetic N$ trade-offs, drift (a physiologically inexpensive, direct escape) should increase under stressful conditions (i.e., reduced pH) if there are no other associated costs. If there are costs to drifting, behaviors other than drifting may be even more sensitive indicators of acid stress in aquatic insects. At low-level pH stress, trade-offs may exist between risks associated with physiological intolerance and predation such that drifting is avoided until physiologically necessary. than 1780 rn (Jensen 1966; Wapd 1985). Like most Here we report the results of a replicated experimental stream emphemerellids, D. coloradensis is a poor swimmer, generally study in which we reduced ambient pH and observed Brunella slow-moving, and exhibits a clinginglsprawling life style coloradensis nymphs for behavioral changes. We predicted that: (Edmunds 1984). Primary food items include diatoms at early (1) nymphal behavior would be influenced by low-level, short- instars and matter during later instaps. In Oregon this tern pH reductions and (%) drifting (a potentially expensive species exhibits a univoltine life history and shows very behavior in terns of predation, but energetically inexpensive) synchronous nymphal growth (Hawkins 1990). Adults emerge would occur more often at the lowest pH levels examined com- in late sumner and early autumn (Jensen 1966; personal pared to lesser pH declines. Our results suggest that nymphal observation). This species occurs in both LB and MC, but in low behavior is influenced by acidity increases, but to different numbers in MC. degrees depending on the severity of pH reductions. We discuss these results in reference to monitoring for acidification effects and Experimental Procedures the implications of behavioral alterations ira response to stress. ccslomdensis nymphs were collected from LB on Study Site and Methods 3 1 July and 6 August 1991. Nymphs were picked from stones using a fine bmsh or forceps, placed in a cooler with LB stream water, and transported to the study reach on MC, nymphs were Site Description placed in in-stream enclosures for at least 48 h prior to use in Two montane streams in the Rocky Mountains of southeast experiments. In-stream enclosures were weighted sieving Wyoming were used; Little Brooklyn Lake irdet (LB) and buckets and contained MC substrate with attached periphyton. Mullen Creek (MC). LB is a second order stream at 3158 rn Only insects that responded to stimulation with a bmsh were elevation in a remote location of the Medicine Bow National used for experiments. Nyn~phswere identified using keys of Forest in southeast Wyoming (4 1'22'8%: 106" 15'N). MC is a first Edmunds (1984) and Ward (1985). order stream at 22572 m elevation located adjacent to the United Experimental stream chmbers were constructed of clear States Forest Service (USFS) research station 1 h west of Plexiglas. The chambers measured 57.0 x 33.5 x 20 cm with a Centennial, WY (41 " 18W, 1106OO9'N). Substrate, flow and water 10-cm collecting basin at each end (Fig. 1). Five panels divided chemistry?especially pH and alkalinity, are similar between the each chamber into six, 5 x 34.5-cm stream channels. A l-m LB and MC sites, which are approximately 10 h apart mesh plastic screen sewed as a barrier on the upper and lower (Table 1). Water chemistry in LB is monitored routinely by channel ends. In each experimental chmber, stream water was USFS personnel as pat of their Glacier Lakes Ecosystem recirculated with a magnetic, centrifugal pump (Little Giant, Experiments Site (GLEES). Model 3-MD-SC) md transferred though a series of Teflon Both sites occur within forest habitat dominated by lodgepole tubes such that channel velocity was within 2 cdssf the velocity pine (Pinus ccbntorta). Ponderosa pine (Pinus ponderma), and at the LB collection site. scattered stands of quaking aspen (Populies trernuksides). Both Thee experimental chambers were imbedded 2-5 cm within sites are fed primarily by snowmelt, but LB has a lake the substrate of MC to maintain slope and contact with approximately 2 h upstream while MC has no upstream lake. surrounding water. Thus the stream served as a bath to maintain MC and LB both contain brook trout populations (Salrno the water temperature within the chambers. Each chamber funeralis). represents one of three pH treatments: an ambient control (pH approx. 8.0). 1 pH unit below ambient, and 2 pH units below Study Organism ambient. Treatments are referred to as C, -I, and -2, respectively. The six channels in each chmber received 2-3 cm of stream The Drunekla coloradensis (Dodds) () substrate (a sand and gravel mixture) that had been sifted to is widely distributed and generally occurs at elevations greater remove any organisms. Chambers were filled with 12 L of MC

Can. J. Fish. Aquat. Sci., kol. 5a3, 1993 ma. 1. Diagram of experimental stream chambers used for exmining behavioral responses to acidification. Chambers are self-contained, recirculating units powered by magnetic, centrifugal pumps. Chamber measurements (length, width, and height) are 5'7.0X 33.5 X 20.0 cm. Each chamber is subdivided into 4 channels measuring 34.5 X 5.0 X 15.0 cm (l,w,h, respectively). There is a 10-cm wide collecting basin at each end of a chamber. The units are placed in-stream for temperature regulation. stream water and the water was circulated in the chmbers for colum. "Crawling" was recorded for a nymph moving across 24 h prior to insect and acid additions. the substrate without visible gill movement. "Ventilating while Each channel received one D. cokoradeszsis nymph (six crawling9'was recorded for nymphs moving across the substrate nymphs per treatment per day). Nymphs were acclimated as while having visible gill fluttering. charnels for 24 h prior to acid additions. At 09:W on 2 and The total frequency of behavioral responses was tested for 8 August enough 0.01 M H,SO, was added to reduce pH levels independence of pH treatment using a Kruskal-Wallis one-way in two chambers -1 and -2 pH units below ambient (control ANOVA. A posteriori multiple comparisons within behaviors pH = 7.79, -1 pH = 7.01, -2 pH = 6.02). Continuous recording were based on a modified Mann-Whitney U-test (Sokal and pH meters (Photovolt Aquacord Model 130) monitored pH Rohlf 198 I). The frequency of behaviors was not significantly levels and manual acid additions were used to maintain pH different between trial days for 16 of 18 comparisons. Because levels. Water samples for chemical analyses were collected from there were only two significant differences, we pooled all each chamber at the start and the conclusion of each experiment. behaviors from the two trial days. We feel pooling caused Samples were analyzed for major anions and cations by the statistical analyses to be more conservative fie., less likely to USFS Water Chemistry Lab in Ft. Collins, C8. show a significant treatment effect if one did not occur) because Scan sampling of behaviors was performed at 5-n9in intervals of the additional variance within cornpaison treatments and was during the first 2 h following acid additions. Scan sampling appropriate in this study. requires an observation of each individual after a fixed mount of time (Martin and Bateson 1986). Because each channel contains only one nymph, an observer could scan each sf the 18 channels (six per treatment) for a nymph, record its behavior, Water chemistry changed as expected after acid additions. and continue though the remaining channels. A "scan9' was Alkalinity and pH levels declined while conductivity and Sod2- completed within 5 fin and the procedure was repeated 25 levels increased (Table 2). Changes in the major cations (Ca2+, times. The behaviors of sitting (s), ventilating (v), burrowing (b), Mg"",a+, and K+) were somewhat erratic, but all generally drifting (4,crawling (c), and ventilating while crawling (vc) increased with acid additions; anions also tended to increase. were recorded. "Sitting" represented a nymph sitting on an Acid treatment influenced the frequency of behaviors exposed substrate surface without movement of the gills or body. displayed by D. coloradensis nymphs, but did not prevent or "Ventilating9' represented a nymph with visible gill movement change any behavior (i.e., nymphs exhibited dl behaviors under sitting on an exposed substrate surface. '6B~rrowing"was all treatments, but at varying frequencies). Fhskal-Wallis recorded for a nymph not visible drifting or visible on the surface ANOVA results suggest that all behavioral frequencies were of any substrate. "Drifting" represented a nymph in the water altered by at least one treatment (Table 3). TABLE2. Water chemistry in experimental chambers before acid additions and after 2-h experiments. The pH was reduced using 0.01 M W2S04. Ions are in geq/E unless stated otherwise. Before After Variable Control - 1 -2 Control - 1 -2

Temperature ("C) Conduct. (pS/crn2)

TABLE3. Mean frequency (?I SE) of observed behaviors for D.co/omden,sis nymphs after acid addition experiments (n = I2 nymphs/treatment). Nymphs were observed at 5-min intervals during the 2-h experiments. Control: pH = 7.8 1, - 1: pH = 7.01, -2: pH = 6.02. See text for explanation sf behaviors. H = bskal-Wallis statistic examining treatment effects on behaviors. *P e 0.05, **Pe0.01, ***IJ e 0.002. Treatment Behavior Control - 1 -2 H

Sit 19.1 (1.25) 8.1 (1.20) 3.2 (0.76) 24.777*** Burrow 1.8 (0.80) 5.0 (1.45) 1.2 (0.64) 8.238* Draft 0.4 (0.22) 0.6 (0.48) 3.7 (1.06) 10.308** Ventilate 0.6 (0.27) 3.3 (0.63) 4.8 (0.80) 18.158*** vc 0.1 (0.08) 0.9 (0.32) 1.5 (8.34) 13.399%" Crawl 2.8 (0.81) 7.1 (1.26) 10.6 (0.82) 15.689*** BEHAVIOR FIG. 2. Within behavior coq~sonsfor Imvd responses to acid additions. Multiple comp~sonswithin behaviors were tested using a modified Mmn-Whitney U-test. Three cs~np~sonswere made for each (vc) showed a similar trend with pH. The -1 and -2 treatment behavior (C vs. -1, C vs. -2, and -1 vs. -2). Smeletters within a behavior nymphs were not significantly different from each other in these indicate the treatments were not different at P < 0.05. See text for thee behaviors. but were different from the controls for these P values of significant differences. On behavior axis, S = sitting; B = behaviors (Cc vs. -Ic, Cc vs. -2c, Cv vs. -Iv, Cv vs. -2v, Cvc vs. burrowing; V = ventilating; C = crawling; v/c = ventilating while -Ivc, Cvc vs. -2vc; &I = 112.0*, 837.5***, 130.5***, 134.5***, crawling; and D = drifting. 109.0*, 128.0**, respectively). Crawling was the most frequent behavior recorded for the -2 nymphs, occurring 42.4% of The frequency of sitting declined with increasing acidity observations. Behaviors of and ;c were never the n~ost (Fig. 2). The control ny tnphs sat more frequently than my other frequently recorded behaviors, but were more frequent for -2 nymphs relative to other treatments (19.2 and 6% respectively). behavior. Control nymphs sat approximately 75% of Drifting behavior occurred more frequently in -2 nymphs than observations and this was more than both -1 and -2 nymphs control and -1 treatments (Mann-Witney U-test, B < 0.05). Drift (Mam-Whitney &I-test,P < 0.001, and P < 0.001 respectively). rates showed an approximately 6-fold increase in the -2 treat- The -1 treatment nymphs also sat more than -2 nymphs ment compared to both - 1 and control treatments. Drifting was (P < 8.635; Fig. 2) and sitting was the most frequent behavior the third most frequent behavior observed in -2 nymphs, but the recorded for the -1 nymphs (about 32% of observations). least frequent behavior in control nymphs (Fig. 2). Drifting Burrowing behavior increased at intermediate acidity levels behavior showed no significant increase at intermediate pH and then declined back to control frequencies at higher acid levels. Drifting was not correlated with crawling for the control, treatment levels (Fig. 2). Bumowing of -I nymphs was greater -1 or -2 treatments (Spearman's rho, all P > 0.05). than both control and -2 nymphs (Mann-Mhitney U-test, P < 0.01 md P < 0.051, but was never the most frequent behavior recorded. Burrowing behavior was recorded for 20% of observations at intermediate pH levels, but less than 10% of The frequencies sf behaviors displayed by D. colo~adensis control and -2 observations. nymphs were influenced by acidity in our experiment and Crawling (c),ventilating (v), and ventilating while crawling depended on the severity of pH reduction. In general, as acidity

Can. J. Fish. Aquaf. Sci., bl. 50, 1993 levels increased, activity levels also increased (e.g., crawling pH stress. Weatherley et al. (1989) showed that pH levels were was more frequent in the treatment chambers than in the positively related to increasing depth within the substrate and controls). Early toxicity research suggested that increased that pH was up to 2 units higher in the substrate than in the activity, including crawling, loss of equilibrium, and drifting, overlying water. This relationship must ultimately depend on the might be a generalized, first response mechanism to nature of the substrate. The value of burrowing as an evasion physiological stress (Yensen and Gaufin 1964a, 1964b; tactic will depend on this and a combination of biotic and abiotic Muirhead-Thonsssn 1978). It is also interesting that endo- factors and their relative costs. Body morphology, nature of the parasitic infections also cause increased activity levels in some substrate, cost of drifting, and predation risks within the substrate mayfly species (Benton and Pritchard 1990). Increased are examples of potential Pactors determining the likelihood of movement patterns ~raightalter interactions between stream burrowing as an escape strategy. In general, smdl-bodied insects by increasing encounter rates with predators (Soluk and nymphs should burrow better than large-bodied nymphs because Collins 1988) or by increasing the probability of abrasion by of access to interstitial spaces. Examination of size distributions water currents (Poff et al. 1991). of drift and benthos between pre- and post-acid additions under Peckaxsky (1988, 1982, 1991) and Beckarsky and Dodson experimental conditions Ilraight address this possibility. Likewise, ( 1980) showed that behavioral interactions (especially predator/ nymphs with hsifom bodies might be expected to bumow better prey) are important in structuring lotic insect comunities under than dorso-ventrally flattened ny~nphs (ice., baetids vs. natural conditions. Behavioral responses to environmental stress heptageniids). Swimming ability and propensity to drift would (especially involving physiological adjustments) may have require attention when interpreting such data. grave implications to these interactions if the species within a The use of inadequate endpoints might lessen our ability to community exhibit some tolerance differences to the stress. For interpret results when monitoring for acidification effects. This example, Wmer et alal.(1993) showed that pH tolerance study suggests that current sampling protocols may, in fact, differences in anuran tadpoles, when combined with population under represent potential impacts and that behaviors may density differences, may alter the outcome of inter- and provide an earlier indication of acid stress in insect communities. intraspecific competition even at pH levels not resulting in death. Routine monitoring of insect comunities for acidification Likewise, elements et al. (1989) showed that sublethal copper effects generally include drift, benthic, and emergence estimates (e.g., Hall et al. 1980). Our results suggest there are lower exposure increased the ability of predatory stoneflies to capture thresholds of stress (i.e., intermediate pH declines influencing netspinning caddis flies because the stoneflies were more behavior) that would not be detected with drift estimates. tolerant of copper than were the caddis larvae. In our experiment, Benthic estimates using Sul-ber-typesamplers give no indication the increased crawling behavior displayed by mayfly nymphs whether insects are hiding in the substratum or normally reside might result in increased encounter rates with predators, reduced there. Possibly, examinations cpf lateral fringe or within-leafpack ability to detect predators, or an increased likelihood of passive comunities would be better methods to estimate refuge seeking drift due to abrasion by currents. If mayfly nymphs are less behavior. Behaviors might also offer useful tools in toxicological tolerant of pH stress than are their stonefly predators, and if a research and field testing for potential hazards by yielding more general response to stress is evasion, stonefly predators might realistic estimates of first-effects concentrations of stressors. experience higher prey capture rates either because of increased Here, using a simple, replicated observation method we have prey encounters or because prey are less capable cpf detecting demonstrated that behavioral responses of a common, lotic predators. mayfly we altered dramatically by a low-level, pH disturbance. As with crawling, increases in drifting rates may influence Regadless of how monitoring protocols are devised in the encounter frequency between species. Drifting frequency future, it is clear that behaviors will have to be incorporated into increased at the lowest pH level examined in our experiment, but sampling designs. not dramatically. Drift responses might have been dampened because the pH reductions in this experiment were not very severe, D. cslcamdensis might be very tolerant of acidity, or drifting may be phylogenetically or morphologically constrained We acknowledge the United States Forest Service through in this species. Also, scan sampling probably gave conservative R. Musselman and L. O'Been for providing lodging and water measurements of drifting behavior because drifting bouts of chemistry analyses. M. Conrad was extremely helpful in collecting shorter duration than scan intervals would be missed. Depending nymphs. A. MeMillan, E. Maurer, and E Wray provided valuable on natural drift distances, short channel length might have led to discussion in preparation of the manuscript. The research was supported an over- or under-estimate of drifting frequency because drifters in part by a Sigma Xi Grant-in-Aid to C. Pennuto and a University of encountered the retaining net. If drift was an active evasion Kinsas, General Research Fund Grant (3 122) to I?. deNoyelles, k tactic, nymphs would be expected to remain on the downstream end of the channels attempting to reenter the water column (i.e., References drifting to avoid stress). Nymphs did not remain on the screen, but generally crawled back to the substrate. ALLAN,J.D. 1978. Trout preddtiom and the size composition of stream drift. Another active behavioa; burrowing, may negate the Lirnnol. Oceamogr. 23: 1231-1237. ALLAN,J.D. 1984. The size cowposition of invertebrate drift in a Rocky consequences of increased crawling and drifting due to acid Mountain stream. Oikos 42: 68-76. stress. At intermediate pH, burrowing may be a pH-stress AI-LARD,M., AND G. MOREABT.1986. Influence sf acidification and aluminum om avoidance behavior that is risk-free in terns of predation if the density and biomass of lotic benthic invertebrates. Water Air Soil Pollut. predators are less able to burrow than are prey. 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