Am. Midi. Nat. (2013) 169:345-353

Laboratory Competition Hierarchies between PotentiallyInvasive Rusty Crayfish (Orconectes rusticus) and Native

Crayfishes of Conservation Concern

KAREN SZELA AND WILLIAM L. PERRY'""̂Department of Biolo^cal Sciences, Behavior, Ecology, Evolution and Systematics Section, Illinois State University,

Normal 61790-4120

ABSTRACT.—Introduced crayfishes represent a serious threat to the endangered aquaticfauna of North America and Europe. We used small-scale competition assay experiments toexamine competitive hierarchies in the laboratory between male and female Orconectes rusticusand Orconectes illinoiensis, Orconectes indianensis, and Orconectes placidus from southern Illinois.These species are considered threatened in Illinois and there is a potential for O. rusticus tobecome established in drainages inhabited by these species. Using sex and size-matchedlaboratory competition trials for a limited food resource, we found that both male and femaleO. rusticus were competitively dominant to O. placidus, O. illinoiensis and O. indianenús (P <0.05). Male 0. placidus, O. illinoiensis, and O. indianensis áhpXsyeA no competitive hierarchies(P > 0.05). Eemale 0. placidus viere, however, competitively dominant to O. illinoiensis whichwas dominant to O. indianensis (P < 0.05). These simple laboratory competition experimentshave been used to explore competition hierarchies involved in both North American andEuropean crayfish invasions to understand observed and potential invasion success. Theseexperiments, although presenting only one small aspect of the many mechanisms involved inthe invasion and displacement of a resident species, can aid in predicting the potential effectsof introduced species prior to an introduction. Our work indicates that the invasion of O.rusticus could have negative consequences for native crayfish species in southern Illinois.

INTRODUCTION

Introduced species can lead to extirpation of resident crayflshes and alter the biodiversityof other components of stream food webs (Charlebois and Lamberti, 1996; Olden et al,2006). Crayfish invasions have occurred within North America and around the globe (Lodgeet al, 2000; Olden et al, 2006; Holdich et al, 2009), and are often facilitated by the bait trade(Taylor et al, 1996). In many lakes and streams of the northeastern United States andsouthern Canada, where the rusty crayfish Orconectes rusticus has been introduced, residentspecies have been driven locally extinct (Buuer and Stein, 1985; Olden et al, 2006).

A wide range of factors can influence the outcome of crayfish invasions. The successfulextirpation of resident species Orconectes propinquus and O. virilis by O. rusticus has beenattributed primarily to the latter's larger body size, faster growth rate, and higher fecundity(Hill et al, 1993). Orconectes rusticus is also less susceptible to prédation than residentcrayfishes due to larger chelae (Roth and Kitchell, 2005). Other North American crayfishes,e.g., Procambarus clarkii and Padfastacus leniusculus, have been introduced into Europe andare vectors of the crayfish plague, Aphanomyces astad, which infects and kills nonresistantEuropean species in most cases but can also displace resident species through ecological

' Present address: Behavior, Ecology, Evolution and Systematics Section, School of BiologicalSciences, Campus Box 4120, Illinois State University, Normal, Illinois 61790-4120. Telephone (309)438-8160; FAX (309)438-8160; e-mail: wlperry@ilstu.edu

^ Corresponding author

345

346 THE AMERICAN MIDLAND NATURALIST 169(2)

mechanisms (Holdich and Domaniewski, 1995; Söderback, 1995; Vorburger and Ribi,1999).

It is important to predict the potential consequences of introduced species before, ratherthan after, an introduction and laboratory experiments can offer some initial insights intopotential species interactions. Laboratory and mesocosm sttidies of competitive hierarchiesand prédation sensitivity have been largely consistent with the observed replacementpatterns in the field (Garvey et al, 1994; Olsen et al, 1991; Roth and Kitchell, 2005).Laboratory experiments have shown that larger Orconectes rusticus were competitivelydominant to smaller O. propinquus for food and shelter, conoborating observeddisplacement patterns of O. propinquus in northern Wisconsin lakes (Hill and Lodge,1999). However, there appears to be population level differences within O. virilis such thatthey are able to coexist with O. rusticus, and laboratory and mesocosm trials examiningcompetition and grovrth rates were consistent with observed patterns in nature (Hayes et al,2009).

Laboratory experiments with Pacifastacus leniusculus, Procambarus clarhii, and several nativeEuropean crayfishes have shown that the North American species were competitivelydominant and posed a significant ecological threat in addition to enabling diseasetransmission (Vorburger and Ribi, 1999; Gherardi and Daniels, 2004; Gherard, 2006).Plague-free populations of P. leniusculus have been found replacing populations of Astacusastacus and Auslropotamobius pallipes, reaffirming that ecological mechanisms identified inthe laboratory may be sufficient for species replacements (Holdich and Domaniewski, 1995;Söderback, 1995). Thus, results from laboratory experiments are often consistent withspecies replacements in nature, even though they represent only one small mechanisminvolved in a species invasion and replacement.

The objective of this study was to use laboratoiy trials to examine competitive hierarchiesin advance of a potential invasion of southern Illinois by Orconectes rusticus. This speciesinhabits the Wabash and Ohio rivers and has the potential to be introduced into southernIllinois (Nonindigenous Aquatic Species Program, USGS, Gainesville, Fl. 1999). Severalstate-threatened crayfishes, O. illinoiensis, O. indianensis, O. kentuckiensis, O. stannardi and O.pladdus, currently occupy southern Illinois streams and are considered at risk of extinction(Page, 1985). If O. rusticus expands its range into this region, the potential for negativeinteractions between the species is possible. It is also possible that the spread of residentcrayfishes in southern Illinois as bait could lead to local extinctions. We utilized methodspreviously used to elucidate the competitive hierarchies among these crayfish species, and,because the native species are ecologically similar to O. propinquus, we hypothesized O.rusticus would be competitively dominant to the crayfishes of southern Illinois: O. illinoiensis,O. indianensis and O. pladdus, in size-matched competition trials for food.

METHODS

Grayfishes from southern Illinois used in the experiment were collected from four OhioRiver tributaries in the Shawnee Hills. These streams are predominately first to third orderwith cobble and boulder substrata with alternating riffles and pools. In May 2001, crayfishwere collected randomly in all habitats of several 300 m sections of each stream drainagetising dip nets and hand collection to avoid size bias (Greed, 1994). Orconectes indianensis v/ascollected from the Haney Greek drainage and O. illinoiensis was collected from the BigGrand Pierre Greek drainage where they are allopatric. O. pladdus was collected from lowersections of the Big Greek drainage and Hogthief Greek where they overlap slighdy with O.kentuckiensis which is found only in the smaller headwater streams (Fig. 1). All individuals

2013 SzELA & PERRY: COMPETITIVE INTERACTIONS BETWEEN CR,\YFISH SPECIES 347

-|- O. indianensisO O. placid us

O. kentuckiensisA O. illinoiensis

FIG. 1.—Inset map of Illinois depicts the isolated collection location of crayfishes in southeasternIllinois. Orconectes indianensis in Haney Cr. and O. illinoiensis in Big Grand Pierre Cr. are allopatric; O.plaädus was collected in lower reaches of Big Cr. and Hogthief Cr., while O. kentuckiensis occupies theheadwaters reaches

were measured to the nearest millimeter, and juveniles less than 20 mm were released. MaleForm I and female crayfish larger than 20 mm were transported to the lab in chilled coolersand each species housed separately in recirculating 150 L aquaria in low densities (<25individuals per tank) with excess shelters. Orconectes rusticus were collected from northernKentucky in Bank Lick Creek (39°0'N, 84°32'W; not shown on the map). Crayfish were fedan ad libitum diet of potatoes, trout chow, and Wardley® Algae Discs. Crayfish were used inexperiments within 2 w of capture.

To test competitive hierarchies between resident crayfishes, Orconectes illinoiensis, O.indianensis, O. pladdus and vnth invading (O. rusticus) crayfish, we used short term, small-scale laboratory experiments modified from Hill and Lodge (1999), Vorburger and Ribi(1999), and Gherardi and Cioni (2006). For each trial, crayfish were placed in plasticcontainers (L X W X H; 30 X 28 X 12 cm) in opposite corners and separated with a clearplasdc divider unül the trial began. The depth of water was maintained at approximately6 cm and the bottom was covered with approximately 1 cm of clean sand. Roomtemperature was maintained at 20 C and the 1212 h light:dark cycle was reversed such thatevening condidons occurred during the day when experiments were conducted.

Crayfish pairs were size-matched to the nearest 0.5 mm and placed together in partitionedcontainers without food for 48 h prior to the experiment and allowed to acclimate to the

348 THE AMERICAN MIDLAND NATURALIST 169(2)

condidons. Sizes of crayfish used in the trials were approximately equally distributedbetween 20 mm and 39 mm. Because crayfish activity peaks around dusk when risk ofprédation is lower, we conducted all trials during the light to dark transidon. During thisperiod, fresh night crawlers (Lumbricus sp.) were cut into 0.5-1 cm secdons and placed in thecenter of container. Then each container was inspected every 10 min with a red coloredflashlight to determine which crayfish obtained the limited resource. The winningindividual was recorded for each container. Experiments lasted until a crayfish possessedthe food resource and this took on average of 1 h with a range from 5 min to 2 h. If theworm was not disturbed or both crayfish were in possession of a piece of worm then the trialwas classified as a tie (Hill and Lodge, 1999); these represented less than 1% of the trials.Dtte to the number of trials and limited space, we ran tbe trials on 3 separate days. May 28,May 30 and June 4, 2001 with roughly equal numbers of each species paired each day andcontainers placed in a random array in the laboratory. Each crayfish was used only one timeand then euthanized, and all containers were bleached, rinsed, and dried between trials.

To test for significant differences of mean crayfish size (carapace length), we used a one-way analysis of variance with a Tukey corrected post F test (Sokal and Rohlf, 2011). To meetassumpdons of normality, data were log transformed and then back-transformed forgraphical presentadon. Outcomes of paired crayfish interacdons were compared againstan expected outcome of equal wins for each species in each pairing scenario usingunreplicated G — tests. In the analysis, des were excluded because tbey were rare (<1%)and there was no basis for generadng expected outcomes in which each individual wascompeddvely equal.

RESULTS AND DISCUSSION

The results of the laboratory competitive hierarchies show that Orconectes rusticus wascompetidvely dominant to O. illinoiensis, O. indianensis, and O. pladdus. For both males andfemales, O. rusticus won significandy more trials versus O. illinoiensis than would be expectedif they were competitively eqtial (n = 19, adjusted G — score = 6.609, P < 0.05; n = 15,adjusted G — score = 8.723, P < 0.05 respectively; Fig 2). Orconectes rusticus males andfemales also won significantly more competition trials versus O. indianensis than would beexpected if they were competidvely equal (n = 15, adjusted G — score = 13.013, P < 0.05; n= 11, adjusted G — score = 4.609, P < 0.05 respectively; Fig. 2). Orconectes rustics wereobsei"ved obtaining the food resource first in most of the trials and even removed the chelaeof the competition in two trials with O. indianensis and one vnth O. illinoiensis. Unfortunatelyduring collections we were unable to collect enough O. placidus that we could pair withequal-sized O. rusticus and could complete only 4 trials, of which O. rusticus won 3 (n = 4,adjusted G — score = 0.930, P > 0.05; Fig. 2). However, in trials between female O. rusticusand O. placidus, O. rusticus won significantly more trials than would be expected if they werecompedtively equal (n = 15, adjusted G — score = 3.397, P < 0.05; Fig. 2).

These small scale, short-term laboratory experiments present only the inidal steps inpredicdng the potendal for Orconectes rusticus to pose a risk to these threatened andendangered species. Similar experiments were used to determine if compeddve hierarchiesbetween O. rusticus and O. propinquus and O. virilis were consistent with observeddisplacement of O. propinquus and O. virilis by O. rusticus (Hill and Lodge 1999). Orconectesrusticus was dotninant to O. virilis, but that only larger O. rusticus were dominant to O.propinquus (Hill and Lodge 1999). Laboratory experiments have been consistent withobserved displacement patterns in lake invasions (Olsen et al, 1991; Hill and Lodge, 1999;Hayes et al, 2009). Similar experiments with invading Padfastacus leniusculus and nadve

2013

100

SzELA & PERRY: COMPETITIVE INTERACTIONS BETWEEN CRAYFISH SPECIES 349

U)

FTG. 2.—Number of laboratory competition trials won for each size-matched (to the nearest mm) O.rusticus with each of O. indianensis, O. illinoiensis, and O. plaädus for males and females. Numbers withinthe bars indicate the number of trials won by the respective species and sex. * indicates significantdifferences using unreplicated G — tests

Austropotamobius torrentium were used to examine mean number of antagonistic interactionsand mean time of sbelter occupancy to determine competitive hierarchies (Vorburger andRibi 1999). Invading P. leniusculus was competitively dominant when equal or larger in sizeto A. torrentium and there was no difference between the trials with males or females(Vorburger and Ribi, 1999). In nature, P. leniusculus has a larger mean size than A. torrentium(Vorburger and Ribi, 1999). Huber and Schubart (2005) have observed poptilations of A.torrentium being displaced by P. leniusculus not carrying the crayfish plague, stiggesting thatlong term displacement can occur, aided by higher fecundity, faster growth rate, and earlierhatching (Vorburger and Ribi, 1999).

We also examined the competitive hierarchies among the southern Illinois species O.illinoiensis, O. indianensis, and O. pladdus to determine if there were potential risks posed byspreading these species among watersheds. The laboratory trials examining competitivehierarchies among males suggested that no single species was competitively dominant insize-matched trials (O. illinoiensis : O. indianensis n = 14, adjusted G — score at 1.119, P >0.05; O. illinoiensis : O. pladdus n = 11, adjusted G — score 0.087, P > 0.05; and O. pladdus :O. indianensis n = 10, adjusted G — score of 0.384, P > 0.05; Fig. 3). These results aresimilar to previous trials in which O. propinquus and O. virilis were competitively equal in thelaboratory, reflecting the alternating dominance of these species in lakes (Hill and Lodge,1999). Interestingly, in trials between native females there were competitive hierarchies with

350 T H E AMERICAN MIDLAND NATURALIST 169(2)

Males Females

*\V jv® *\V jv©

0- 0-̂ 0' 0-̂

Males Females

0* 0-

Males Females

FIG. S.—Number of laboratory competition trials won for each size-matched (to the nearest mm) pairsof 0. indianensis, O. illinoiensis, and O. placidus for males and females. Numbers within the bars indicatethe number of trials won by the respective species and sex. * indicates significant differences usingunreplicated G-tests

O. pladdus dotninating O. illinoiensis (n = 6, adjusted G — score 7.678, P < 0.05; Fig. 3) andO. illinoiensis dominating O. indianensis females (n = 8, adjusted G — score = 4.764, P <0.05; Fig. 3). Due to limited numbers of individuals we could not test O. pladdus and O.indianensis. In southern Illinois, the significantly larger O. pladdus would likely displace theboth smaller species O. illinoiensis and O. ¿ncí¿ara«rei¿i which may elicit alternating dominance.It is unclear why competitive hierarchies of females differed from males. Prior competitionexperiments have focused on male Orconectes (Hill and Lodge, 1999) even though female O.rusticus appeared to lead the invasion in Trout Lake, Wisconsin (Perry et al, 2001). It ispossible that the role of female Orconectes may be more important than previously thought.

Competitive superiority in most experiments has been attributed to larger size except in alimited number of experiments (Gherardi and Cioni, 2004). In most experiments as the sizeof the invader increased to reflect the mean size difference in nature, the relativedominance of the invader increased (Hill and Lodge, 1999; Vorburger and Ribi, 1999). Insouthern Illinois, we observed significant size differences among the crayfishes withOrconectes rusticus frotn its native range being larger on average than all other species exceptO. pladdus (F7478 = 26.95, P < 0.0001) (Fig. 4). The mean size of O. rusticus and O. pladdusdid not differ significantly (P > 0.05; Fig. 4). Female O. rusticus were not significantlydifferent from male O. illinoiensis, but were larger than female O. illinoiensis (P < 0.05;Fig. 4). Male and female O. illinoiensis did not differ in size from male O. indianensis

2013 SzELA & PERRY: GOMPETITIVE INTERACTIONS BETWEEN GRAYFISH SPECIES 351

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35 -

• j : 30

i 25 i(Od. 20

15

10

5A46

A,B46 85

C100

C44

wD44

A45

A76

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Males Female

O. illinoiensis

Males Female

O. indianensisMales Female

O. placidus

FIG. 4.—Carapace lengths of male and female (least square means +/— 1 standard error) of O. nisticus(Bank Lick Cr, Kentucky) and O. illinoiensis, 0. indianensis, and O. pladdus from southeastern Illinois(Fig. 1). Data were back-transformed from log-transformed data. Different letters indicate significantdifferences between species X sex categories (P < 0.05)

(P > 0.05) but were larger than female O. indianensis, which were smaller than all otherspecies (P < 0.05; Fig. 4). Again, due to the status of these crayfish, we were unable toconduct trials reflecting size differences observed in the field. However, we might predictlarger 0. rusticus would be relatively more dominant over 0. illinoiensis and O. indianensis,but dominance hierarchies may differ for O. pladdus from the laboratory trials. Among thenative species, O. pladdus is the largest and there size may confer a competitive advantageover O. illinoiensis cind especially over the small O. indianensis.

These experiments are only an initial step in trying to understand potential outcomesshould Orconectes rusticus spread into these systems. Most stLidies have suggested that thesesimple competition experiments are consistent with displacement patterns in the field(Vorburger and Ribi, 1999; Hill and Lodge, 1999; and Gherardi and Gioni, 2006), althoughin one invasion scenario, observed displacements in the field could not be replicated inmesocosm experiments (Larson and Magoulick, 2009). Prédation can also be an importantcomponent in species invasions, particularly when refugia are limited. These crayfishesinhabit smaller streams that may not have large predatory fish populations, and refugiaappeared to be unlimited. Gompetition in nature may, however, be less intense thanobserved in laboratory trials (Bergman and Moore, 2003) due to excess shelters and food.Fecundity, survivorship, and growth rates have been shown to be key factors in the successesof invasive species, but the life history of these species has not been systematically examined.Fecundity is related to crayfish size and thus the larger O. rusticus and O. pladdus may havehigher fecundities than O. illinoiensis and O. indianensis.

352 THE AMERIC^AN MIDLAND NATURALIST 169(2)

Our study provides preliminary evidence for the potential consequences of an Orconectes

rusticus invusion in southern Illinois. Several native crayfishes {e.g., O. pladdus, O. indianensis,

0. illinoiensis, O. kentuckiensis, and O. stannardî), that have small populations and limiteddistributions inhabit this region, are considered at risk of extirpation. Our laboratoryexperiments have shown that O. rusticus is competitively dominant to O. pladdus, O.

indianensis, and O. illinoiensis. As found iti other studies (Vorburger and Ribi, 1999; Gherardiand Cioni, 2006; Gherardi, 2006), these assay experiments can provide insight intointeractions between native and nonnative crayfish. Our results indicate that there is thepotential for O. rusticus to become dominant should this species be introduced to southernIllinois and highlights the potential risk to the endemic crayfish in this region.

Acknowledgments.—We would like to thank the School of Biological Sciences and Illinois StateUniversity for funding and the Department of Natural Resources for allowing us to collect thecrayfishes. This manuscdpt also benefitted greatly from comments by two anonymous reviewers andDavid Berg, associate editor.

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