Some Phoretic Associations of Macroinvertebrates on Transplanted Federally Endangered Freshwater Mussels

Abstract

Benthic macroinvertebrates were washed from nearly 1000 federally endangered freshwater mussels that had been collected from Pennsylvania during a reintroduction project to 2 eastern Illinois streams. Most benthic macroinvertebrates collected were larvae of the Neophylax fuscus, but other caddisflies and segmented worms were also observed. No unoccupied caddisfly cases were observed on live mussels, leaving open the question as to the seasonal fate of these microhabitats after caddisflies pupate and emerge in the fall each year. Unionid mussel shells might modify local-scale species diversity by influencing physical and hydraulic properties of microhabitats.

Full text

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Northeastern Naturalist Notes
2017 Vol. 24, No. 4
J.L. Robinson, M.J. Wetzel, and J.S. Tiemann
Some Phoretic Associations of Macroinvertebrates on Transplanted Federally
Endangered Freshwater Mussels
Jason L. Robinson1,*, Mark J. Wetzel1, and Jeremy S. Tiemann1
Abstract - Benthic macroinvertebrates were washed from nearly 1000 federally endangered fresh-
water mussels that had been collected from Pennsylvania during a reintroduction project to 2 eastern
Illinois streams. Most benthic macroinvertebrates collected were larvae of the Neophylax fuscus, but
other caddisies and segmented worms were also observed. No unoccupied caddisy cases were ob-
served on live mussels, leaving open the question as to the seasonal fate of these microhabitats after
caddisies pupate and emerge in the fall each year. Unionid mussel shells might modify local-scale
species diversity by inuencing physical and hydraulic properties of microhabitats.
Life-history knowledge gaps. Basic attributes of macroinvertebrate life histories are
often poorly known and under-reported in the scientic literature. Gaps in the informa-
tion on the ecology of individual organisms are one of a number of knowledge gaps that
systematically limit the effective management and conservation of species, as well as our
understanding of the factors that constrain species diversity and the evolution of new traits
and taxa (Cardoso et al. 2011, Hortal et al. 2015). The prospect of improving the manage-
ment of species under special conservation protections provides an additional impetus for
reporting basic life-history and ecological attributes of these species, and the other mem-
bers of the ecological communities in which they persist.
Relocation project. Beginning in 2005, biologists from the Illinois Natural History
Survey (INHS) partnered with personnel from the US Fish and Wildlife Service and from
several state resource management agencies in Ohio and Pennsylvania to rescue indi-
viduals of 2 federally endangered mussel species, Epioblasma rangiana (Lea) (Northern
Rifeshell) and Pleurobema clava (Lamarck) (Clubshell). The mussels were collected from
the footprint of a proposed bridge construction on the Allegheny River in Forest County,
PA, in areas of swiftly owing water with clean and stable sand, gravel and cobble sub-
strates (Stodola et al. 2017, Tiemann 2014). Mussels were relocated to the Vermilion River
basin in Champaign and Vermilion counties, IL, with the goal of re-establishing viable
populations of these 2 species into areas where they were considered extirpated (Cummings
and Mayer 1997, Tiemann 2014). This paper concerns macroinvertebrates collected from
live mussels transplanted during 26–27 August 2013.
Individual mussels (249 Northern Riffleshell and 758 Clubshell) were quarantined
in a holding facility at the University of Illinois at Urbana-Champaign (UIUC), tagged
with passive integrated transponder (PIT) tags, and then resituated at 8 different sites in
the Middle Fork (5) and Salt Fork (3) of the Vermilion River (Stodola et al. 2017, Tie-
mann 2014). During tagging, the external shell of individual mussels was scrubbed and
temporarily dried to facilitate the attachment of tags. This process rinsed and removed
attached sediment and epibionts, including caddisfly cases and other aquatic macro-
invertebrates. Most of this material was retained in 95% ethanol for later microscopic
inspection and identification.
We identied 152 individual macroinvertebrates, representing 4 species (Table 1). The
macroinvertebrates we report herein are a nonrandom and limited subset of the complete
1Illinois Natural History Survey, Prairie Research Institute at the University of Illinois Champaign-
Urbana, Champaign, IL 61820. *Corresponding author - jrob@illinois.edu.
Manuscript Editor: Trip Krenz
Notes of the Northeastern Naturalist, Issue 24/4, 2017

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J.L. Robinson, M.J. Wetzel, and J.S. Tiemann
phoretic fauna associated with these 2 mussel species, because many organisms were
certainly detached or disassociated during the process of removal and quarantine.
Life history and local ecology. Both of the mussel species considered here are typically
found in medium to large rivers in clean, stable sand, gravel, and cobble rifes, where they
may live several inches beneath the streambed surface (Cummings and Mayer 1992, Wat-
ters et al. 2009). These 2 species vertically migrate to the streambed surface during their
reproductive period; Northern Rifeshell are bradytictic (brooding from September to the
following June), whereas Clubshells are tachytictic (brooding from early May to July). The
macroinvertebrate assemblage associated with the shells of these 2 mussel species could be
different during these reproductive periods compared to the rest of the year. Associations
of macroinvertebrates and unionids within this interstitial microhabitat are likely to experi-
ence temporal progression within each year, as a function of mussel vertical migration and/
or macroinvertebrate life history (e.g., adult emergence of Neophylax sp. in autumn).
Table 1. List of macroinvertebrates dislodged from 249 Epioblasma torulosa rangiana (Northern Rif-
eshell) and 758 Pleurobema clava (Clubshell) from the Allegheny River (Route 62 Bridge, 4.5 km
SW Tionesta, Forest County, PA, 41.472348°N, 79.499838°W), collectors J.S. Tiemann, K.S. Cum-
mings, S.A. Douglass, A.L. Price, et al.
Phylum Class Order Family Species Count
Arthropoda Insecta Trichoptera Thremmatidae Neophylax fuscus 113
Arthropoda Insecta Trichoptera Leptoceridae Oecetis inconspicua 2
Annelida Clitellata Rhynchobdellida Glossiphoniidae Helobdella papillata 35
(Hirudinea)
Annelida Clitellata Tubicida Naididae Nais bretscheri 1
Annelida Clitellata Tubicida Naididae Unidentied Naidinae 1
Figure 1. Ventral view of N. fuscus case, with larva enclosed. Remnants of mussel shell are visible at
anterior and posterior attachment sites.

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J.L. Robinson, M.J. Wetzel, and J.S. Tiemann
Neophylax cases are tube-like, typically with large stones anking the tube along the axis
of the body of the organism (Fig. 1). The insect prepares for pupation by enclosing the tube
and rmly attaching the larval case to some rm substrate (including mussel shells) with silk
produced from glands located in the mouth of the larva (Sehnal and Akai 1990). Cases may
persist, in some habitats, for several years after the emergence of adults. Larvae occupied all
cases removed from mussels in this study, and no empty cases from previous seasons were ob-
served. This nding is curious because Neophylax fuscus Banks cases were so rmly attached
to mussels that removing the cases during our prepping procedure also removed small pieces
of periostracum (the non-living outer layer of the shell) at the attachment sites (Fig. 2). Law-
eld et al. (2014) suggested that Trichoptera case attachment might not harm or damage the
shell of mussels because this attachment is conned to the periostracum.
The aquatic annelids rinsed from external mussel shells included the leech Helobdella
papillata (Moore; 5 brooding adults, 5 non-brooding adults, and 25+ young of the year that
had detached from parents), one aquatic oligochaete (Nais bretscheri Michaelsen) and one
other unidentied naidid oligochaete (Table 1). Several leech species in the family Glos-
siphoniidae (including H. papillata) are known associates of freshwater mollusks, feeding
primarily if not exclusively on mollusks (Sawyer 1986). Several species in the oligochaete
genus Chaetogaster (most commonly, Chaetogaster limnaei von Baer) are often collected
from pulmonate snails (externally, from within the mantle cavities, around the apertures,
and as parasites in the kidneys; Klemm 1985), from unionid bivalves (externally and from
within the mantle cavities; Anderson and Holm 1987, Beckett et al. 1996, Kelly 1988), and
occasionally from freshwater sponges, bryozoans, and crayshes (Sawyer 1986; Stephen-
son 1930; Wetzel et al. 2009; M.J. Wetzel, pers. observ.).
Surprisingly, no Chaetogaster specimens were present in the material washed from the
mussels from our study, but as noted above, many organisms were certainly detached or
Figure 2. Close up view of remnants of freshwater mussel shell remaining at the posterior attachment
site on a N. fuscus case.

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J.L. Robinson, M.J. Wetzel, and J.S. Tiemann
disassociated during the process of removal and quarantine. Neither Nais bretscheri nor
other congeners in the genus are known to have commensal or parasitic relationships with
mollusks. It is possible that aquatic oligochaetes washed from the mussels were living
within silt and sand on the shell of the mussels, and also possible that these individuals were
only incidentally using areas around caddisy cases as habitat or refugia. We note a litany
of personal eld and lab experience on oligochaetes and other macroinvertebrate fauna in
the contents of caddisy cases or puparia, which frequently contain more macroinvertebrate
species when examined in detail (Beckett et al. 1996; Bodis et al. 2014; Laweld et al. 2014;
J.L. Robinson and M.J. Wetzel, pers. observ.; pers. comm. from caddisy taxonomists D.
Denson [Reedy Creek Improvement District, Lake Buena Vista, FL), C. Parker [ret. USGS,
Gatlinburg, TN], D. Etnier [ret. UT-Knoxville, Knoxville, TN], and D. Ruiter [ret. USEPA,
Centennial, CO]) and sometimes provide a substrate for Podostemum ceratophyllum Mi-
chx. (Hornleaf Riverweed) (Vaughn et al. 2002).
Among our observations, all cases we report were occupied by living caddis, and
older cases from which caddis had previously emerged were completely absent. Little
is known about the behaviors or ecological significance of burrowing mussels (New-
ton et al. 2015). Although mussels are known to vertically migrate to escape predation
(Burlakova et al. 2000) and control zebra mussel infestation (Nichols and Wilcox 1997),
we hesitate to speculate that vertical migration can remove spent cases. Regardless,
caddisfly cases may help to create and maintain fine-scale structural and hydraulic and
ecological diversity widely reported from freshwater mussel habitats (Commito and Ru-
signuolo 2000, Gutierrez et al. 2003, Lawfield et al. 2014, Taniguchi and Tokeshi 2004,
Vaughn and Spooner 2006).
We believe that this report is the rst literature discussion of a phoretic association
between living unionid mussels and any of the conrmed eastern North American species
of Neophylax (Trichoptera: Thremmatidae) in the ecological literature. However, phoretic
associations of Trichoptera with unionids have been reported from fossils dating to the Pa-
leocene of North Dakota, where psychomyiid caddisy retreats and net were preserved on a
unionid (Erickson 1983). Trichoptera associations must be known or familiar to malacolo-
gists who observe organisms in the eld, and associations with case-building Trichoptera
have previously been suggested from photographs of organisms attached to dead shells
(Laweld et al. 2014), but not identied to genus or species. Images posted on the USFWS
website for this specic project clearly depicted Neophylax cases on specimens in situ,
and images published in Laweld et al. (2014) suggest hydropsychids, hydroptilid, and
glossosomatid caddisies may successfully colonize the surface of unionids. Interestingly,
Anderson and Vinikour (1984) reported the use of unionid mussels and viviparid snails as
pupation sites for the leptocerid caddisy Oecetis inconspicua (Walker), but no associations
with other extant Trichoptera species have yet been reported. Interspersed among Neophy-
lax cases were 2 very early instar larvae of some species of Oecetis, in the O. inconspicua
group (Floyd 1995)—instars that could not be condently associated with any of the mor-
phologically distinguishable forms within this group.
Although interesting as ecological trivia, this observation raises issues about quar-
antine and unionid reintroduction efforts. Our results are at best an underestimate of the
fauna attached to or living on the mussels in situ but a great example of how organisms
can unintentionally be transported great distances. Predicting which species might be
most likely to be introduced might prove difficult, because numerous observations of
epibiotic relations suggest that many different taxa can form these associations without
specificity (Wahl and Mark 1999). Caddis cases, or macrophytes, might be obvious to

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J.L. Robinson, M.J. Wetzel, and J.S. Tiemann
most observers and frequently removed during basic quarantine. Oligochaetes or other in-
vertebrates inhabiting the mantle cavities or internal organs of mollusks, as well as those
capable of hiding in the crevices of the shells, may be more difficult or impossible to posi-
tively remove. The chance for accidental introduction of non-native macroinvertebrates
obviously increases when hundreds, if not thousands, of mussels are translocated into
new river basins across multiple years. To avoid potential contamination and unwanted
introduction of macroinvertebrates, careful, stringent quarantine procedures should be
considered when transporting freshwater mussels.
Acknowledgments. This relocation project is being funded, in part, by a natural resource damage
assessment settlement (Hegeler Zinc–Lyondell Basell Companies) to the US Fish and Wildlife Service
(USFWS) and to the State of Illinois. USFWS, Pennsylvania Fish and Boat Commission (PFBC), and
Illinois Department of Natural Resources (IDNR) issued collecting permits. Staff and volunteers from
EnviroScience (Ohio), IDNR, Illinois Natural History Survey, Ohio State University, Columbus Zoo
and Aquarium (Ohio), PFBC, Prairie Rivers Network, USFWS, and West Virginia Department of Nat-
ural Resources assisted with collecting and scrubbing mussels. Dead mussel specimens, trichopterans
and annelid specimens identied during this study are deposited, respectively, in the INHS Mussel, In-
sect, and Annelid Collections (Epioblasma rangiana- INHS 46825, Pleurobema clava- INHS 46829,
Neophylax fuscus- INHS 797483, Oecetis inconspicua group- INHS 797484, Helobdella papillata
INHS_ANNELID_10269_431, Nais bretscheri INHS_ANNELID_10270_164, unidentied Naidinae
INHS_ANNELID_10271_102).
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