First record of phoresy between chironomid larvae and crayfish.
Abstract: Multiple specimens of the rusty crayfish (Orconectes rusticus) collected from the Susquehanna River in Pennsylvania exhibited Rheotanytarsus sp. (Diptera: Chironomidae) living on their carapaces and chelipeds. Although chironomid larvae have been reported as living on many aquatic organisms, this is the first record of chironomids living phoretically on crayfish.
Article Type: Report
Subject: Chironomids (Physiological aspects)
Larval development (Physiological aspects)
Crayfish (Physiological aspects)
Authors: Mangan, Brian P.
Bilger, Michael D.
Pub Date: 04/01/2012
Publication: Name: The American Midland Naturalist Publisher: University of Notre Dame, Department of Biological Sciences Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Earth sciences Copyright: COPYRIGHT 2012 University of Notre Dame, Department of Biological Sciences ISSN: 0003-0031
Issue: Date: April, 2012 Source Volume: 167 Source Issue: 2
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 287956861
Full Text: INTRODUCTION

Phoresy is a term generally used to describe the attachment of a nonparasitic animal to another animal (Svensson, 1979; Prat et al., 2004). This attachment is practiced by some aquatic dipterans among the Chironomidae, Simuliidae, and Ceratopogonidae. Chironomid phoresy has been reported on many types of aquatic organisms and this association is thought to provide these midges with food resources, substrate, and dispersal mechanisms (McCafferty, 1981). In some instances phoretic associations have been re-evaluated and judged to be parasitic (Jacobsen, 1998).

Chironomid larvae have often been found living on the larvae of mayflies. Wilda (1987) discovered Rheotanytarsus sp. (Chironominae: Tanytarsini) encased on the thorax of Tricorythodes sp. (Leptohyphidae). The incidence of chironomids on mayflies in Czech streams was related to chironomid density (Soldan, 1988). In a Brazilian stream the chironomid Nanocladius (Orthocladiinae) were observed attached dorso-laterally in silk nets between the thorax and abdomen of the mayfly Thraulodes (Leptophlebiidae) (Callisto and Goulart, 2000). Larvae of the mayfly Ephemera guttulata (Ephemeridae) have been reported to host as many as three species of Orthocladiinae midges (Jacobsen, 1995). Pepinelli et al. (2009) observed simuliid pupae and larvae, and chironomid larvae, living on mayfly larvae in South America and concluded that these associations were opportunistic.

Researchers have concluded that some Nanocladius live parasitically on their insect hosts. Jacobsen (1998) observed that the gut contents of Nanocladius larvae and scarring of host tissue suggested that these chironomids were feeding primarily on the hemolymph of their mayfly hosts. A parasitic relationship between an undescribed Nanocladius sp. and the stonefly Pteronarcys biloba (Pteronarcyidae) was confirmed by stable isotope analysis (Doucett et al., 1999). Caldwell and Wiersema (2002) also reported probable evidence of parasitism by N. bubrachiatus on the leptophlebiid mayfly Traverella presidiana in a Texas stream.

Other commonly reported insect hosts include megalopterans. Almost two-thirds of the hellgrammites (Corydalus cornutus) from a Tennessee stream carried chironomids (Furnish et al., 1981). Similar phoretic relationships with C. cornutus were also reported in Missouri (Tracy and Hazelwood, 1983), Costa Rica (De La Rosa, 1992) and Maine (Pennuto, 1997). Larval and pupal Nanocladius asiaticus were reported on both dobsonfly and fishfly larvae in Japan, but some of these midges died when the larval megalopterans exited the water to pupate in riparian soils (Hayashi, 1998). Hayashi and Ichiyanagi (2005) demonstrated that chironomid attachment sites on the megalopteran Protohermes grandis were a function of the number of midges living on the host and smaller midges were forced to live in less preferred locations on the host. Brazilian researchers reported that larvae of Nanocladius (Plecopteracoluthus) living phoretically on Corydalus sp. were also a common prey of this megalopteran (Callisto et al., 2006).

Odonates and coleopterans have also been reported to host chironomids. As many as 71% of the larvae of the dragonfly Boyeria vinosa, collected from a stream in South Carolina, had larvae of Rheotanytarsus sp. attached to them (White et al., 1980). In Hong Kong, host dragonflies of Zygonyx iris had an average of 3.5 chironomids attached to their legs, thoracic nota, and wing sheaths (Dudgeon, 1989). The damselfly Argia moesta were also reported to host larvae of the chironomid Nanocladius branchicolus in an Ontario stream (Dosdall and Parker, 1998). Segura et al., (2007) observed Rheotanytarsus sp. living on an adult riffle beetle (Hexacylloepus) in Brazil.

Noninsect hosts of chironomids include snails (Mancini, 1979; White et al., 1980; Prat et al., 2004), mussels (Ricciardi, 1994) and fish (Roque et al., 2004; Sydow et al., 2008). We report the first record of chironomid phoresy involving crayfish. These specimens were collected during a survey of crayfish of the Susquehanna River in Pennsylvania.

METHODS AND MATERIALS

Crayfish were sampled at 11 locations along a 400 km section of the Susquehanna River from the New York border to near Harrisburg, Pennsylvania. The survey was conducted between Jun, and Sept. 2008. We set 100 baited wire traps at each location. Our traps were designed and built specifically for the capture of crayfish (Mangan et al., 2009a, b). All of the crayfish specimens were preserved in 70% ethanol for later identification and morphometric measurements. Peckarsky et al. (1990) and Nuttall (2008) were used to identify crayfish. Ali specimens were deposited in the permanent collection of the Susquehanna Steam Electric Station Environmental Laboratory.

RESULTS

We captured 804 crayfish from among the 11 sampling locations. Two species of crayfish were collected at the sites, the native Allegheny crayfish (Orconectes obscurus, n = 209) and the invasive rusty crayfish (O. rusticus, n = 591). At only one location (Sunbury, Lat: 40[degrees]50'26"N, Long: 76[degrees]51'21"W) did we capture three specimens of O. rusticus with larvae of Rheotanytarsus sp. living on them, less than 0.4% of the total number of crayfish captured from the river. Five of the 86 crayfish collected at this site were O. obscurus, but no chironomids were observed on these specimens.

The number of chironomid cases on crayfish ranged from 2 to 10, with a total of 16 cases among three Orconectes rusticus specimens. Ten cases were found on the largest crayfish, a female with a carapace length of 36.1 mm. Four cases were observed on a male with a carapace length of 91.1 mm, and two cases were observed on a female with a carapace length of 21.9 mm. Only four cases contained specimens of Rheotanytarus sp., the remaining cases were empty.

Eight of the chironomid cases occurred within the cervical ridge on the dorsal or lateral surface of the carapace. Two cases were on the side of the carapace above the third and fourth sets of walking legs. Four of the cases were observed on the ventral surface of the merus or the dorsal surface of the carpus of the chelae. In addition, one case was located along a postorbital ridge and another on the rostrum (Fig. 1).

Not all of these cases contained chironomid larvae; therefore, we cannot be certain if a different midge had built each one, Some of the cases appeared to have been either abandoned before they were completed or older cases that had fallen into disrepair after abandonment.

DISCUSSION

To our knowledge there are no previously published reports of chironomid phoresy among crayfish. Given the abundance of reports of chironomid phoresy among other aquatic animals, particularly those examples involving Rheotanytarsus sp., their discovery on crayfish is not surprising. What is surprising, however, particularly in light of the research emphasis on freshwater crayfish ecology and biodiversity, is that it has taken so long to be reported. One likely factor in the delay of this discovery is that many crayfish researchers do not preserve their specimens, but instead identify, measure, and release them alive in the field. In these instances it would be very difficult to observe small chironomid cases on living specimens, particularly when the crayfish were still wet. This would also be true of preserved specimens that were studied before the exoskeleton of crayfish specimens had sufficiently dried. In fact, it was not until the exoskeletons of our specimens had air-dried that we first noticed the chironomid cases using stereomicroscopy. Any future attempts to study the incidence of chironomid phoresy on crayfish should keep these limitations in mind.

Many cases (10) were observed on the largest crayfish we collected and multiple cases were observed on all three specimens. Larger crayfish offer greater substrate area for chironomid attachment, and as a result can conceivably host more larvae. De La Rosa (1992) reported larger megalopterans hosting more chironomids than smaller larvae. Furthermore, the occupation of a larger host should decrease the likelihood of competition for preferred sites on hosts as reported by Hayashi and Ichiyanagi (9005). Our observations of multiple cases on each crayfish, as well as within certain locations of the crayfish, e.g., the cervical ridge, suggest that competition could influence case placement. Therefore, it is entirely possible that competition is also at work for case placement on crayfish hosts, particularly among smaller crayfish specimens.

Chironomids have been reported to position themselves on hosts to avoid commonly groomed areas (Hayashi, 1998; Hayashi and Ichiyanagi, 2005). All of the chironomid cases on crayfish seemed to occur in positions that would escape grooming. Crayfish have been reported to be able to rid themselves of epibionts by grooming, at least to a limited degree, but molting is the surest way to completely clear themselves of attached organisms (Holdich, 2002).

[FIGURE 1 OMITTED]

Rheotanytarsus sp. have been reported to build cases from materials ranging from sand grains and mud particles to diatoms (Saether and Kyerematen, 2001). In a study of macroinvertebrate colonization of acrylic plates anchored to the bottom of the Susquehanna River, Deutsch (1980) reported that Rheotanytarsus sp. was the most abundant taxon present and comprised 40% of the total organisms on the plates. Furthermore, 97% of the Rheotanytarsus observed favored colonization of the plate tops rather than the bottoms.

For larval Rheotanytarsussp. to attach to a crayfish two major steps seem necessary. The first step involves accessing the crayfish. This seems most likely to be accomplished by larvae crawling onto a crayfish from the benthic substrate. White et al. (1980) postulated that motionless periods by larval dragonflies while hunting provided chironomids the opportunity to build cases on these larvae. Less likely, but also plausible, a chironomid larva suspended in the water column could drift onto a crayfish. Once on a crayfish, the second major step would involve selecting a location to build a case. The locations on the host would need to be areas where chironomids could have access to the material needed for case construction, likely benthic sediments or particulates suspended in the water column. White et al. (1980) noted that chironomid (primarily Rheotanytarsus) phoresy on benthic macroinvertebrates was relatively common in streams with sandy bottoms. They suggested that midge larvae were building cases on benthic macroinvertebrates because of a lack of hard surfaces such as rocks for attachment. Another explanation, however, might be the availability of the fine sandy sediments suspended in the water column that provide the larvae on the macroinvertebrates the materials for building cases. One of the noticeable characteristics of the site where we collected our specimens was the greater abundance of sand in the substrate as compared to the other sampling locations. This sampling site was approximately 1 km downstream of an inflatable dam on the Susquehanna River. The dam is used between May and Oct. each year to provide water recreation on a river normally too shallow for these activities. When the dam is inflated, strong water currents below the dam can suspend sandy sediment in the water column, perhaps creating the conditions for successful case building.

It is thought that the benefits of phoresy for chironomids include a host substrate with fewer competitors, ample food resources and a mechanism for dispersal (McCafferty, 1981; Tokeshi, 2006). Dosdall and Parker (1998) cited the benefits of phoresy for Nanocladius branchicolus to include better substrate stability in fast currents, energy savings for relocation, less interspecific competition and improved pupation sites. The sites selected by Rheotanytarsus sp. on the crayfish could provide feeding benefits for this genus of passive filter-feeders (Wallace and Merritt, 1980). The cervical ridge bisecting the carapace was the most preferred site for the chironomids occupying our specimens, containing half of the observed cases. Three other locations occurred on the dorsal surface of the crayfish included the rostrum, postorbital ridge area and the carpus of the chelid. These locations would also provide the suspension-feeding larvae of Rheotanytarsus sp. ample access to sediments suspended in the water column. Given the mobility of crayfish chelae in the water column, this would also be true for those cases located on the dorsal surface of the merus.

Tokeshi (2006) concluded that phoresy practiced by the Chironomidae provided a strategy for these midges to overcome limits of mobility and to decrease predation. In particular, he noted that larger hosts decreased the vulnerability of chironomids to freshwater predators that are generally "gape limited." This conceptual advantage needs to be tested, however. Arguably, it is just as likely that chironomids attached to crayfish are substituting one group of freshwater predators for the predators of the crayfish. In addition, the reliability of crayfish as a host substrate is questionable in light of regular molting of the host exoskeleton. It would seem that attachment to a crayfish exoskeleton soon to be molted offers less benefit than attachment to a recently molted crayfish, especially if, as occurs in some crayfish species, the exoskeleton will be consumed by the crayfish.

This report is the first to document chironomid phoresy on crayfish. The overall incidence of this relationship throughout the Susquehanna River and elsewhere remains to be measured, as do the environmental conditions that contribute to it.

LITERATURE CITED

CALDWELL, B. A. AND N. A. WIERSEMA. 2002. New records and observations for parasitic chironomid midges (Diptera: Chironomidae) and their mayfly (Ephemeroptera) hosts. Ent. News, 113:11-14.

CALUSTO, M. AND M. D. C. GOULART. 2000. Phoretic association between Nanocladius (Plecopteracoluthus) sp. (Chironomidae: Diptera) and Thraulodes sp. (Leptophlebiidae: Ephemeroptera). An. Soc. Entomol. Brasil, 29:605-608.

--, --, P. MORENO AND R. P. MARTINS. 2006. Does predator benefits prey? Commensalism between Corynoneura Winnertz (Diptera, Chironomidae) and Corydalus Latreille (Megaloptera, Corydalidae) in Southeastern Brazil. Rev. Bras. Zool., 23:569-572.

DE LA ROSA, C. L. 1992. Phoretic associations of Chironomidae (Diptera) on Corydalidae (Megaloptera) in northwestern Costa Rican streams. J. N. Am. Benthol. Soc., 11:316-323.

DEUTSCH, W. G. 1980. Macroinvertebrate colonization of acrylic plates in a large river. Hydrobiologia, 75:65-72.

DOUCETT, R. R., D. A. GIBERSON AND G. POWER. 1999. Parasitic association of Nanocladius (Diptera: Chironomidae) and Pteronarcys biloba (Plecoptera: Pteronarcyidae): insights from stable-isotope analysis. J. N. Am. Benthol. Soc., 18:514-523.

DOSDALL, L. M. AND D. W. PARKER. 1998. First report of a symphoretic association between Nanocladius branchicolus Saether (Diptera: Chironomidae) and Argia moesta (Hagen) (Odonata: Coenagrionidae). Am. Midl. Nat., 139:181-185.

DUDGEON, D. 1989. Phoretic Diptera (Nematocera) on Zygonyx iris (Odonata: Anisoptera) from a Hong Kong river: incidence, composition, and attachment sites. Arch. Hydrobiol., 115:433-439.

FURNISH, J., D. BELLUCK, D. BAKER AND B. PENNINGTON. 1981. Phoretic relationships between Corydalus cornutus (Megaloptera: Corydalidae) and Chironomidae in Eastern Tennessee. Ann. Entomol. Soc. Am., 74:29-30.

HAVASHI, F. 1998. Nanocladius (Plecopteracoluthus) asiaticus sp. n. (Diptera: Chironomidae) phoretic on dobsonfly and fishfly larvae (Megaloptera: Corydalidae). Aquat. Insects, 20:215-229.

--AND H. ICHIYANAGI. 2005. Density dependent shifts in attachment site by the ectosymbiotic chironomid Nanocladius asiaticus on its megalopteran host Protohermes grandis. Entomol. Sci., 8:253-261.

HOLDICH, D. M. 2002. Background and functional morphology, p. 3-29. In: D. M. Holdich (ed.). Biology of freshwater crayfish. Blackwell Science, Oxford.

JACOBSEN, R. E. 1995. Symbiotic associations between Chironomidae (Diptera) and Ephemeroptera, p. 317-332. In: L. D. Corkum and J.J.H. Ciborowski (eds.). Current directions in research on Ephemeroptera. Canadian Scholars' Press, Toronto.

--. 1998. The symbiotic relationship of a chironomid with its Ephemeropteran (caps?) host in an Arizona mountain stream. J. Kansas Entomol. Soc., 71:426-438.

MANCINI, E. R. 1979. A phoretic relationship between a chironomid larva and an operculate stream snail. Ent. News., 90:33-36.

MANGAN, B. P., A. D. CILIBERTO AND M. T. HOMEWOOD. 2009a. A versatile and economical trap for capturing wild crayfish. J. Freshw. Ecol., 24:119-124.

--, J.J. SAVITSKI AND N. T. FISHER. 2009b. Comparison of two traps used for capturing wild crayfish. J. Freshw. Ecol., 24:445-450.

McCAFFERTY, W. P. 1981. Aquatic entomology: The fisherman's and ecologist's illustrated guide to insects and their relatives. Jones and Bartlett Publishers, Sudbury, Massachusetts. 448 p.

NUTTALL, T. 2008. Key to PA crayfishes. Available from: http://www.lhup.edu/tnuttall/pennsylvania_ crayfish_reference_.htm. Accessed 2008 Jun. 11.

PECKARSKY, B. L., P. R. FRAISSINET, M. A. PENTON AND D.J. CONKLIN. 1990. Freshwater macroinvertebrates of northeastern North America. Cornell University Press, Ithaca, New York.

PENNUTO, C. M. 1997. Incidence of chironomid phoretics on hellgrammites in streams of southern Maine. Northeast. Nat., 4:285-292.

PEPINELLI, M., T. SIQUEIRA, F. F. SALES AND E. M. SHIMBORI. 2009. First report of Simuliidae and Chironomidae (Diptera) living on nymphs of Lachlania Hagen (Ephemeroptera: Oligoneuriidae) in South America. Biota Neotrop, 9:245-247.

PRAT, N., D. ANON-SUAREZ AND M. RIERADEVALL. 2004. First record of Podonominae larvae living phoretically on the shells of the water snail Shilina dombeyana (Diptera: Chironomidae/ Gastropoda: Lymnaeidae). Aquat. Insects, 26:147-152.

ROQUE, F. O., M. TRIVINHO-STRIXINO, M.JANSCO AND E. N. FRAGOSO. 2004. Records of Chironomidae larvae living on other aquatic animals in Brazil. Biota Neotr., 4:1-9.

RICCIARDI, A. 1994. Occurrence of chironomid larvae (Paratanytursus sp.) as commensals of dreissenid mussels (Dreissena polymorpha and D. bugensis). Can. J. Zool., 72:1159-1162.

SAETHER, O. A. AND R. A. KYEREMATEN. 2001. Towards phylogeny and zoogeography of the genus Rheotanytarus Thieneman et Bause, 1913 (Diptera: Chironomidae.). Tijdschr. Entomol., 144: 73-117.

SEGURA, M. O., A. A. FONSECA-GESSNER AND T. C. A. BATISTA. 2007. Phoretic association between larvae of Rheotanytarsus and adult Coleoptera, collected from State Park Campos do Jordao, Srio Paulo State, Brazil. Rev. Bras. Zool., 24:503-504.

SOLDAN, T. 1988. Distributional patterns, host specificity and density of an epoictic midge, Epoicocladium ravens (Diptera, Chironomidae) in Czechoslovakia. Vest. ds. Spolec. zool., 52:278-289.

SVENSSON, B. S. 1979. Pupation, emergence, and fecundity of phoretic Epoicodadius epheraerae (Chironomidae). Holarct. Ecol., 2:41-50.

SYDOW, V. G., F. S. VILELLA, S. M. HARTZ AND G. G. RODRIGUES. 2008. Ichthyocladius (Diptera, Chironomidae) on loricariid fishes in Atlantic Forest streams: influence of host size and corporal region on larval attachment. Acta Limnol. Bras., 20:333-337.

TOKESHI, M. 2006. On the evolution of commensalisms in the Chironomidae. Freshw. Biol., 29:481-489.

TRACY, B. H. AND D. H. HAZELWOOD. 1983. The phoretic association of Urnatella gracilis (Entoprocta: Urnatellidae) and Nanoeladius downesi (Diptera: Chironomidae) on Corydalus cornutus (Megaloptera: Corydalidae). Freshwat. Invertebr. Biol., 2:186-191.

WALLACE, J. B. AND R. W. MERRITT. 1980. Filter-feeding ecology of aquatic insects. Ann. Rev. Entomol., 25:103-132.

WHITE, T. R., J. S. WEAVER III AND R. C. Fox. 1980. Phoretic relationships between Chironomidae (Diptera) and Benthic Macroinvertebrates. Entomol. News, 91:69-74.

WILDA, T.J. 1987. Notes on phoresy between Rheotanytarsus sp (Diptera: Chironomidae) and Tricorythodes sp. (Ephemeroptera: Trichorythidae) in a South Carolina tailwater stream. Entomol. News, 98:159-160.

BRIAN P. MANGAN (1), Environmental Program, King's College, Wilkes-Barre, Pennsylvania 18711; and MICHAEL D. BILGER, EcoAnalysts Inc., Selinsgrove, Pennsylvania 17870. Submitted 11 March 2010; Accepted 25 October 2011.

(1) Corresponding author: Telephone (570) 208-5900; e-mail: brianmangan@kings.edu
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