Distribution and Habitat of the Endemic Earthworm
Eisenoides lonnbergi (Michaelsen) in the Northeastern
United States
Timothy S. McCay, Rebecca A. Pinder, Eric Alvarado, and Watson C. Hanson
Northeastern Naturalist, Volume 24, Issue 3 (2017): 239–248
Full-text pdf (Accessible only to subscribers. To subscribe click here.)
Access Journal Content
Open access browsing of table of contents and abstract pages. Full text pdfs available for download for subscribers.
Current Issue: Vol. 30 (3)
Check out NENA's latest Monograph:
Monograph 22
Northeastern Naturalist Vol. 24, No. 3
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017
239
2017 NORTHEASTERN NATURALIST 24(3):239–248
Distribution and Habitat of the Endemic Earthworm
Eisenoides lonnbergi (Michaelsen) in the Northeastern
United States
Timothy S. McCay1,*, Rebecca A. Pinder2, Eric Alvarado1, and Watson C. Hanson1
Abstract - Eisenoides lonnbergi is one of just a few native earthworm species known from
north of the most recent glacial maximum and has been found most commonly in saturated
soils. We sampled earthworms from wetlands in Upstate New York and compiled published
and unpublished records of E. lonnbergi to better describe the distribution and habitat associations
of this species in the Northeast. We found E. lonnbergi at 14 of 22 sampled sites,
including 8 of 14 riparian areas and 6 of 8 wetlands of other types (bogs, fens, and swamps).
Soil pH at colonized sites varied from 3.4 to 8.5. At the 3 most acidic sites, E. lonnbergi
was the only species detected by our sampling. Published records with habitat data also support
an association between E. lonnbergi and wetland habitats of variable pH, both above
and below the most recent glacial maximum. Eisenoides lonnbergi is strongly associated
with wetlands, including some habitats, such as acidic bogs, in which it may be the only
earthworm present. Land managers and conservation biologists should consider Eisenoides
lonnbergi along with other native species sensitive to the loss of wetlands in the Northeast.
Introduction
Approximately one-third of earthworm species found in North America north
of Mexico are believed to have been introduced from Europe and Asia (Blakemore
2008, Hendrix et al. 2008, Reynolds 1995). In particular, non-native taxa
dominate the earthworm fauna of previously glaciated northeastern North America
(Hendrix and Bohlen 2002, Reynolds 2010, 2016). Of those species hypothesized
to be endemic to eastern North America, only 4 have been documented north of
the southern limit of the most recent glacial maximum: Bimastos parvus (Eisen),
B. tumidus (Eisen), Eisenoides lonnbergi (Michaelsen), and Sparganophilus eiseni
Smith (Reynolds 2010). Interestingly, these species all seem to be associated with
mesic habitats, at least in the Northeast (James 1995, Reynolds 2010), suggesting
either that mesic habitats represent a refuge for native earthworms within an upland
landscape dominated by exotics or that mesic habitats may have been more conducive
to dispersal and recolonization following glacial retreat.
Eisenoides lonnbergi has been called a “semi-aquatic species” (James 1995)
and a “freshwater oligochaete” (Tillinghast and Huffman 1973). It is known primarily
from wetlands with saturated soils and has been collected from muddy
substrates beneath standing water (Gates 1955, James 1995). This species has
1Department of Biology, Colgate University, Hamilton, NY 13346. 2Division of Science,
Columbia-Greene Community College, Hudson, NY 12534. *Corresponding author -
tmccay@colgate.edu.
Manuscript Editor: Peter K. Ducey
Northeastern Naturalist
240
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017 Vol. 24, No. 3
been collected in both acidic (pH < 5; Wherry 1924) and basic (pH > 8; James
1995) wetland soils, where animals are likely in direct, continuous contact with
soil water. These findings suggest a breadth in pH tolerance that is unusual for
lumbricid earthworms (Satchell 1955). Eisenoides lonnbergi has been collected
in swamps, marshes, bogs, and along the banks of streams and rivers (e.g., Davies
1954, Gates 1935, Reynolds 2002). Thus, E. lonnbergi seems to exhibit broad
habitat tolerances within wetland ecosystems.
Knowledge of E. lonnbergi in the Northeast has come from just a few studies and
relatively few sites. Gates (1972) regarded their presence in southern New England
as likely the result of recent transportation by humans, and as recently as 2010
E. lonnbergi was documented at only a single site in New York State (Reynolds
2008, 2010; Schwert 1976). James (1995) summarized our understanding of the
distribution of this species and indicated a distribution extending significantly into
Massachusetts and New York. However, prior to the current work, the northernmost
record for this species, in Oswego County, NY, was thought questionable because
its location near a public fishing area made it a likely bait introduction (Schwert
1976). Ecological studies of earthworms in saturated soils have been less frequent
than studies in upland habitats. Thus, the paucity of records for E. lonnbergi may
be due to lack of scientific attention, an actual uncommonness, or both.
The specific epithet for this species has been reported elsewhere as lönnbergi
(e.g., Gates 1955) and loennbergi (Szlávecz and Csudi 2007). We report it here
as lonnbergi (without the umlaut). Lonnbergi is a latinized Swedish surname
(Lönnberg), and the International Code of Zoological Nomenclature (Article
32.5.2.1) specifies that diacritical marks should be removed from scientific
names (International Commission on Zoological Nomenclature 1999). Because it
is a Swedish, rather than German, surname, no “e” should be added after removal
of the umlaut.
We report here on new records of E. lonnbergi from wetlands and riparian habitats
in New York State. These samples were taken well north of the southern limit
of the last glacial advance, and several samples are farther north than all published
records except the Oswego County, NY, sample of Schwert (1976). These new records
shed additional light on the distribution, prevalence, and habitat associations
of E. lonnbergi.
Methods
Sites and earthworm sampling
We collected E. lonnbergi during a study of earthworms in riparian habitats of
eastern New York State in 2006–2008 and during earthworm surveys of wetland
habitats in central New York in June and July of 2016. Seven headwater streams
were selected in each of Catskill State Park, Greene County, and Edmund Niles
Huyck Preserve, Albany County. Additional information about these sites is available
in Pinder (2013). During the summer of 2016, we sampled earthworms at 8
wetland habitats (bogs, fens, and swamps) in Madison and Chenango counties, New
York, which were publically owned or owned by a land trust.
Northeastern Naturalist Vol. 24, No. 3
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017
241
Earthworms in wetlands can be difficult to detect due to the saturated soils of
these habitats. Common techniques, such as mechanical (Springett 1981) or chemical
(Lawrence and Bowers 2002) extraction, were not used to avoid damage to
sensitive wetland environments. We used time-constrained searching, a technique
commonly used to sample amphibians (Heyer et al. 1994), to sample earthworms.
We spent a minimum of 2 person-hours of time in our efforts to find earthworms at
each site.
Structures at the soil surface, including rocks and logs, were flipped and then
returned to their original position. When structures were not present, we manipulated
the substrate by hand while looking for earthworms. We searched for animals
under leaf litter and moss (if present) and within the underlying soils to a depth
of about 10 cm. In sphagnum bogs, we would only minimally disrupt vegetation,
instead spending most of our time watching the surface for signs of movement. At
streamside sites we would systematically move along the stream bank searching for
earthworms under rocks and logs. Because our sampling methods differed among
habitats, we could not assume equal probability of detecting E. lonnbergi at all
sites. Furthermore, weather likely influenced detection probabilities. Therefore, we
avoided making inferences regarding the abundance of animals detected, and the
described distribution should be viewed as conservative. Sampled earthworms were
placed in plastic containers with substrate from the collection site and transported
to the lab for processing.
Environmental measurement
At each location, we measured the pH of the substrate of sampled habitats. For
habitats with free water at the surface (e.g., sphagnum bogs and fens), we would
simply collect and measure the pH of free surface water. When surface water was
not available, pH of the soil was measured using the method described in Carter
(1993). We used a Bluelab® pH meter (Bluelab® Corporation Ltd., New Zealand) to
measure pH.
Processing of specimens
We first examined collected worms alive, making notes about behavior and pigmentation,
and photographed them when possible for later reference. Earthworms
were euthanized in 10% isopropanol, fixed in 10% formalin for at least 48 hours,
and then stored in 70% isopropanol. Processing was completed in 15-ml plastic
centrifuge tubes, and earthworms were stored and labeled individually. We identified
the earthworms by examination of external characters and use of Reynolds
(1977) and Schwert (1990) and accessioned specimens into the oligochaete collection
of the Museum of the Chenango Valley at Colgate University.
Review of published and unpublished records
We used literature databases (BioOne®, JSTOR®, Web of Sciencetm Core Collection)
as aids in compiling published records of E. lonnbergi in Connecticut,
Maryland, Massachusetts, New Jersey, New York, Pennsylvania, Rhode Island,
and West Virginia. State-specific review articles by Reynolds (e.g., 2002)
Northeastern Naturalist
242
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017 Vol. 24, No. 3
provided a useful guide to the literature in these states. We attempted to find,
without success, published records in Maine, New Hampshire, and Vermont. We
searched the holdings of E. lonnbergi at the National Museum of Natural History
(http://collections.nmnh.si.edu) and the Museum of Comparative Zoology at Harvard
(http://mczbase.mcz.harvard.edu/). We additionally solicited unpublished
records of E. lonnbergi from colleagues sampling earthworms in the Northeast.
We did not confirm determinations for records that were not our own, and in one
instance (Genesee County, NY, unpubl. record) we accepted an uncollected sighting
of a specimen as a record.
We estimated the geographic coordinates of each collection or sighting using the
published description, field notes, or, if no specific information was available,
the centroid of the county in which the specimen was collected. We recorded the
habitat description indicated in the original account for each record and made particular
note of any indication that the specimen(s) had been collected from soils
that were saturated at the time of collection or other habitat or vegetation descriptors
that would indicate collection from a wetland (e.g., “from sphagnum peat”).
Collections made at the edge of a water body (e.g., “at edge of small pond”) were
considered to have come from a wetland habitat.
Results
We collected E. lonnbergi from 14 new locations in New York State: 8 streamside
sites, 3 bogs, and 3 forested wetlands (Table 1). All locations were glaciated
during the last glacial maximum (Fig.1) and include the most northerly records
for this species aside from the published record in Oswego County, NY (Schwert
1976). We found E. lonnbergi in 8 of 14 streamside sites (Pinder 2013) and 6 of
8 bogs, fens, and swamps. Our sites varied widely in pH (3.4 to 8.5), supporting
claims that this species has a broad pH tolerance (e.g., James 1995). At our 3 most
acidic sites (e.g., Fiddler’s Green Bog), E. lonnbergi apparently did not coexist
with any other species (Table 1), suggesting that E. lonnbergi may be unique among
earthworms of the Northeast in its tolerance of acidic saturated substrates.
At riparian areas, E. lonnbergi was found with a wide variety of earthworm species
(Table 1). Indeed, riparian habitats may support a uniquely diverse earthworm
assemblage in the Northeast (Pinder 2013). At non-riparian habitats, E. lonnbergi
was found with Allolobophora chlorotica (Savigny), Dendrobaena octaedra
(Savigny), Eiseniella tetraedra (Savigny), Lumbricus rubellus Hoffmeister, and
Octolasion tyrtaeum (Savigny). These species all have been found in a range of
habitats, including environments that were either moist or acidic (or both), in previous
studies (e.g., Zorn et al. 2008).
We found 57 published records and 5 unpublished records of E. lonnbergi in
Connecticut, Delaware, Massachusetts, Maryland, New Jersey, New York, Pennsylvania,
Rhode Island, and West Virginia representing 62 distinct sites at which
E. lonnbergi was collected (for detail of all records north of the southern limit of
the last glacial maximum, see Supplemental File 1, available online at https://www.
eaglehill.us/NENAonline/suppl-files/n24-3-N1544-McCay-s1, and, for BioOne
Northeastern Naturalist Vol. 24, No. 3
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017
243
Table 1. Sites at which we collected Eisenoides lonnbergi in New York State, along with a description of habitat and coexisting species identified. We
measured pH of either free surface water, if any, or the soil at the site in which the species was found.
Site name Habitat type pH Coexisting species
Broadstreet Hollow, Catskill State Park (CSP), Riparian 5.2 (10) Aporrectodea caliginosa, A. limicola, A. rosea,
Greene County A. tuberculata, Dendrobaena octaedra, Eiseniella tetraedra,
Lumbricus rubellus, L. terrestris, Octolasion cyaneum, O. tyrtaeum
Fiddler’s Green, Madison County Sphagnum bog 3.8 (0)
Great Swamp Conservancy, Madison County Swamp 8.5 (2) Allolobophora chlorotica, L. rubellus
Grevatt Road, Edmund Niles Huyck Preserve Riparian 6.0 (14) Aporrectodea caliginosa, A. limicola, A. rosea,
(ENHP), Albany County A. trapezoides, A. tuberculata, Dendrobaena octaedra,
Dendrodrilus rubidus, Eisenia fetida, Eiseniella tetraedra,
L. castaneus, L. rubellus, L. terrestris, O. cyaneum, O. tyrtaeum
Hunter Mountain, CSP, Greene County Riparian 4.4 (8) Aporrectodea trapezoides, A. rosea, A. tuberculata,
Dendrobaena octaedra, Dendrodrillus rubidus, L. rubellus,
O. cyaneum, O. tyrtaeum
Jam Pond, Chenango County Sphagnum bog 3.6 (0)
Lost Pond, Madison County Margin of sphagnum bog 4.6 (3) Dendrobaena octaedra, L. rubellus, O. tyrtaeum
Mink Hollow, CSP, Greene County Riparian 4.4 (7) Aporrectodea tuberculata, A. rosea, A. turgida, Dendrobaena
octaedra, Dendrodrillus rubidus, L. rubellus, O. tyrtaeum
Nelson Swamp Unique Area, Madison County Forested fen 6.8 (3) Eiseniella tetraedra, L. rubellus, O. tyrtaeum
North South Lake, CSP, Greene County Riparian 5.1 (9) Aporrectodea rosea, A. tuberculata, Dendrobaena octaedra,
Dendrodrillus rubidus, Eiseniella tetraedra, D. octaedra,
D. rubidus, L. rubellus, O. tyrtaeum
Pond Trail, ENHP, Albany County Riparian 5.0 (11) Aporrectodea caliginosa, A. limicola, A. rosea,
A. trapezoides, A. tuberculata, Dendrobaena octaedra,
Dendrodrillus rubidus, Eiseniella tetraedra, L. rubellus,
L. terrestris, O. tyrtaeum
Route 42, CSP, Greene County Riparian 5.3 (8) Aporrectodea rosea, A. tuberculata, Dendrobaena octaedra,
Dendrodrillus rubidus, Eiseniella tetraedra, L. rubellus,
O. cyaneum, O. tyrtaeum
Shooter, CSP, Greene County Riparian 5.5 (6) Aporrectodea tuberculata, Dendrobaena octaedra,
Dendrodrillus rubidus, L. rubellus, O. cyaneum, O. tyrtaeum
Stone Barn State Forest, Oneida County Swamp 3.4 (0)
Northeastern Naturalist
244
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017 Vol. 24, No. 3
subscribers, at https://dx.doi.org/10.1656/N1544.s1). Thirty-four of these records
included detailed habitat or soils information. The large majority of records indicated
a wetland habitat (30; 88%), with the largest number of collection sites
characterized as riparian habitat (16; 47%), followed by swamps and marshes (9;
26%), lake-sides (4; 12%), and a bog (1; 3%). The 4 upland sites were all forested
and included a Populus (aspen) forest (Schwert 1976), Pinus strobus L. (White
Pine)–Tsuga (hemlock) forest (Gates 1935), and a mixed mid-Atlantic deciduous
forest (Szlávecz and Csuzdi 2007, Szlávecz et al. 2011). In particular, E. lonnbergi
is abundant and persistent at upland sites within the Smithsonian Environmental
Research Center (SERC) in Maryland (Szlávecz and Csuzdi 2007). These SERC
sites (Treefall, Triangle, and Weir; Yesilonis et al. 2016) have well-drained soils
with a litter layer dominated by Liriodendron tulipifera L. (Tulip Poplar) and Fagus
grandifolia Ehrh. (American Beech), indicating that at least certain populations of
Figure 1. Locations at which Eisenoides lonnbergi were collected in the current study and
in published and unpublished accounts. Shaded area was redrawn from the distribution
described in James (1995) based on information available at that time. Line represents the
southern limit of the Wisconsinan glaciation (Garrity and Soller 2009). Published records
are plotted for Connecticut, Delaware, Massachusetts, Maryland, New Jersey, New York,
Pennsylvania, Rhode Island, and West Virginia. Unpublished records in New York State
were provided by A.M. Pagano and P.K. Ducey (State University of New York at Cortland,
Cortland, NY) and S.W. James (University of Iowa, Iowa City, IA); unpublished record
in Pennsylvania was provided by A.J. Britson (The Pennsylvania State University, State
College, PA); unpublished records in Connecticut were provided by J.P. Fischer (White
Memorial Conservation Center, Litchfield, CT).
Northeastern Naturalist Vol. 24, No. 3
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017
245
E. lonnbergi are physiologically tolerant of upland conditions (K. Szlávecz, Johns
Hopkins University, Baltimore, MD, pers. comm.).
Published accounts similarly mention wetland characteristics north of (13 of 16
sites) and south of (17 of 18 sites) the southern limit of the last glacial maximum.
Thus, habitat selection seems similar in areas overwhelmingly dominated by exotic
species and in areas with greater representation of nearctic earthworms.
Discussion
These new records underscore the prevalence of E. lonnbergi in the northern
reaches of its described range and expand the known geographic distribution to the
northwest. Importantly, these new records occur above the glacial margin. Many
of these records occurred in remote habitats not adjacent to public fishing areas or
other likely sources of recent human-aided colonization. We therefore argue that
E. lonnbergi has naturally colonized Upstate New York following glacial retreat.
The current limits to the geographic distribution of this species are unclear.
Olson (1940), Eaton (1942), and Reynolds (2008) did not find Eisenoides at many
collection sites in western and northern New York, but their sites were almost exclusively
in upland habitats. So, the occurrence of E. lonnbergi farther to the north
or west is still uncertain. This species has now been confirmed to exist in watersheds
that drain northward, toward Lake Ontario, and earthworms may be passively
dispersed by freshwater streams (Costello et al. 2011, Schwert and Dance 1979).
Therefore, we predict that E. lonnbergi will be found at other locations in northern
New York. Intentional sampling of wetland habitats will be necessary to clearly
define the distribution of this species.
Eisenoides lonnbergi was collected at over 60% of our sampled wetlands, suggesting
that it may be relatively common in habitats with saturated soils in central
and eastern New York. Nevertheless, this species is clearly uncommon in nonsaturated
soils. In a study of 75 upland sites in southern Madison County, NY, we
collected no E. lonnbergi (T. McCay, unpubl. data). Other studies of the earthworm
faunas of upland habitats in New York have similarly detected no E. lonnbergi
(Bernard et al. 2009, Stegman 1960).
As reported previously (James 1995), our data indicate that E. lonnbergi is
tolerant of very acidic conditions as well as neutral to slightly basic conditions.
Satchell (1955) classified earthworms on the basis of pH tolerance and identified
“ubiquitous” earthworms that were present in soils varying from pH 3.7 to pH
8.8. Eisenoides lonnbergi apparently exhibits a similarly broad range of pH tolerance.
Its tolerance of acidic, saturated conditions may in fact be unique among
earthworms in the Northeast. At our most acidic wetlands, we collected no other
co-occurring species, including species identified by Satchell (1955) as ubiquitous
and found in the region, such as Lumbricus rubellus. However, our sampling methodology
was particularly aimed at E. lonnbergi and may have underrepresented
other species, particularly Sparganophilus eiseni, which can be found at greater
depths and in more saturated conditions than E. lonnbergi (Harman 1965, Pinder
2013). Eisenoides lonnbergi may possess an unusual physiological ability to
Northeastern Naturalist
246
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017 Vol. 24, No. 3
tolerate these saturated acidic conditions or, perhaps, it has an unusual ability to
forage in these habitats dominated by Sphagnum mosses. Chang et al. (2016) used
isotope analysis to demonstrate that E. lonnbergi occupied a distinctive trophic
niche compared to other syntopic species. Additional research into the physiology
and ecology of E. lonnbergi is necessary to resolve these uncertainties.
Because it is so closely linked to wetland habitats and is among only a few
representatives of the nearctic earthworm fauna in the Northeast, land managers
may want to consider E. lonnbergi among other wetland endemics. In particular,
E. lonnbergi may be the only oligochaete in acidic wetlands, such as bogs, a fact
that may strengthen arguments for conservation based on the distinctiveness of
these habitats. We encourage earthworm biologists to sample earthworms in nontraditional
environments in northern North America. It is within marginal habitats
(e.g., wetlands) and microhabitats (e.g., under bark) that northern native species
are predominantly found (James 1995). Additional sampling is needed before we
can construct an accurate understanding of the northern edge of the distribution of
Eisenoides lonnbergi, and other native earthworms, in North America.
Acknowledgments
S.E. Scanga, S.E. Dexter, E.A. Hutto, A.O. Nugent, and V.C. Escobar provided help in
the field and lab. Special thanks to A.J. Britson, P.K. Ducey, J.P. Fischer, S.W. James, and
A.M. Pagano for sharing data regarding field collections of Eisenoides lonnbergi. We are
grateful to the New York State Department of Environmental Conservation, the Southern
Madison Heritage Trust, and the Cazenovia Preservation Foundation for allowing access to
properties. The Upstate Institute at Colgate University provided funding in support of this
project. The first and second authors contributed equally to this work
Literature Cited
Bernard, M.J., M.A. Neatrour, and T.S. McCay. 2009. Influence of soil buffering capacity
on earthworm growth, survival, and community composition in the western Adirondacks
and central New York. Northeastern Naturalist 16:269–284.
Blakemore, R.J. 2008. A series of searchable texts on earthworm biodiversity, ecology, and
systematics from various regions of the world. 3nd Edition. Available online at http://
www.annelida.net/earthworm. Accessed 1 November 2016.
Carter, M.R. (Ed.). 1993. Soil Sampling and Methods of Analysis. CRC Press, Boca Raton,
FL. 823 pp.
Chang, C.-H., K. Szlávecz, T. Filley, J.S. Buyer, M.J. Bernard, and S.L. Pitz. 2016. Belowground
competition among invading detritivores. Ecology 97:160–170.
Costello, D.M., S.D. Tiegs, and G.A. Lamberti. 2011. Do non-native earthworms in southeast
Alaska use streams as invasional corridors in watersheds harvested for timber?
Biological Invasions 13:177–187.
Davies, H. 1954. A preliminary list of the earthworms of northern New Jersey, with notes.
Breviora 26:1–13.
Eaton, T.H., Jr. 1942. Earthworms from the northeastern United States: A key with distribution
records. Journal of the Washington Academy of Sciences 32:242–249.
Garrity, C.P., and D.R. Soller. 2009. Database of the geologic map of North America;
adapted from the map by J.C. Reed Jr. and others (2005). United States Geological Survey
Data Series 424. Available online at https://pubs.usgs.gov/ds/424/.
Northeastern Naturalist Vol. 24, No. 3
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017
247
Gates, G.E. 1935. The earthworms of New England. Proceedings of the New England Zoological
Club 15:41–44.
Gates, G.E. 1955. Notes on American earthworms of the family Lumbricidae I–II. Breviora
48:1–12.
Gates, G.E. 1972. Contributions to North American earthworms (Annelida), No. 4. On
American earthworm genera. I. Eisenoides (Lumbricidae). Bulletin of Tall Timbers
Research Station 13:1–17.
Harman, W.J. 1965. Life-history studies of the earthworm Sparganophilus eiseni in Louisiana.
Southwestern Naturalist 10:22–24.
Hendrix, P.F., and P.J. Bohlen. 2002. Exotic earthworm invasions in North America: Ecological
and policy implications. Bioscience 52:801–811.
Hendrix, P.F., M.A. Callaham, Jr., J.M. Drake, C.-Y. Huang, S.W. James, B.A. Snyder, and
W. Zhang. 2008. Pandora’s Box contained bait: The global problem of introduced earthworms.
Annual Review of Ecology, Evolution, and Systematics 39:593–613.
Heyer, R.W., M.A. Donnelly, R.W. McDiarmid, L.C. Hayek, and M.S. Foster (Eds.). 1994.
Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians.
Smithsonian Institution Press, Washington, DC. 364 pp.
International Commission on Zoological Nomenclature. 1999. International Code of Zoological
Nomenclature. 4th Edition. The International Trust for Zoological Nomenclature,
London, UK. 306 pp.
James, S.W. 1995. Systematics, biogeography, and ecology of nearctic earthworms from
eastern, central, southern, and southwestern United States. Pp. 29–51, In P.F. Hendrix
(Ed.). Earthworm Ecology and Biogeography. CRC Press, Inc., Boca Raton, FL. 244 pp.
Lawrence, A.P., and M.A. Bowers. 2002. A test of the “hot” mustard extraction method of
sampling earthworms. Soil Biology and Biochemistry 34:549–552.
Olson, H.W. 1940. Earthworms of New York State. American Museum Novitates 1090:1–9.
Pinder, R.A. 2013. Ecology of earthworms in riparian habitats. Ph.D. Dissertation. University
at Albany, State University of New York, Albany, NY. 101 pp.
Reynolds, J.W. 1977. The earthworms (Lumbricidae and Sparganophilidae) of Ontario.
Life Sciences Miscellaneous Publication of the Royal Ontario Museum, Toronto, ON,
Canada. 162 pp.
Reynolds, J.W. 1995. Status of exotic earthworm systematics and biogeography in North
America. Pp. 1–27, In P.F. Hendrix (Ed.). Earthworm Ecology and Biogeography. CRC
Press, Inc., Boca Raton, FL. 244 pp.
Reynolds, J.W. 2002. Additional earthworm records from Rhode Island (Oligochaeta: Lumbricidae
and Megascolecidae). Megadrilogica 9:21–27.
Reynolds, J.W. 2008. The earthworms (Oligochaeta: Lumbricidae, Megascolecidae, and
Sparganophilidae) of New York, USA, revisited. Megadrilogica 12:1–17.
Reynolds, J.W. 2010. Earthworms (Oligochaeta: Acanthodrilidae, Lumbricidae, Megascolecidae
and Sparganophilidae) of northeastern United States, revisited. Megadrilogica
14:101–157.
Reynolds, J.W. 2016. Earthworms (Oligochaeta: Lumbricidae, Megascolecidae and Sparganophilidae)
in the Northeastern Highlands Ecoregion (58), USA. Megadrilogica
19:222–231.
Satchell, J.E. 1955. Some aspects of earthworm ecology. Pp. 180–201, In D.K. McE. Kevan
(Ed.). Soil Zoology. Academic Press, Inc., London, UK. 512 pp.
Schwert, D.P. 1976. Recent records of earthworms (Oligochaeta: Lumbricidae) from central
New York State. Megadrilogica 2:7–8.
Northeastern Naturalist
248
T.S. McCay, R.A. Pinder, E. Alvarado, and W.C. Hanson
2017 Vol. 24, No. 3
Schwert, D.P. 1990. Oligochaeta: Lumbricidae. Pp. 352–355, In D.L. Dindal (Ed.). Soil
Biology Guide. Wiley-Interscience, New York, NY. 1349 pp.
Schwert, D.P., and K.W. Dance. 1979. Earthworm cocoons as a drift component in a southern
Ontario stream. Canadian Field-Naturalist 93:180–183.
Springett, J.A. 1981. A new method for extracting earthworms from soil cores, with a
comparison of four commonly used methods for estimating earthworm populations.
Pedobiologia 21:217–222.
Stegman, L.C. 1960. A preliminary survey of earthworms of the Tully Forest in Central New
York. Ecology 41:779–782.
Szlávecz, K., and C. Csuzdi. 2007. Land-use change affects earthworm communities in
eastern Maryland, USA. European Journal of Soil Biology 43:S79–S85.
Szlávecz, K., M. McCormick, L. Xia, J. Saunders, T. Morcol, D. Whigham, T. Filley, and
C. Csuzdi. 2011. Ecosystem effects of non-native earthworms in Mid-Atlantic deciduous
forests. Biological Invasions 13:1165–1182.
Tillinghast, E.K., and D.G. Huffman. 1973. The pattern of nitrogen excretion during fasting
of two fresh-water oligochaetes. Comparative Biochemistry and Physiology A
45:555–557.
Wherry, E.T. 1924. Acidity preferences of earthworms. Ecology 5:309.
Yesilonis, I., K. Szlávecz, R. Pouyat, D. Whigham, and L. Xia. 2016. Historical land-use
and stand-age effects on forest soil properties in the Mid-Atlantic US. Forest Ecology
and Management 370:83–92.
Zorn, M.I., C.A.M. Van Gestel, E. Morrien, M. Wagenaar, and H. Eijsackers. 2008. Flooding
responses of three earthworm species, Allolobophora chlorotica, Aporrectodea caliginosa,
and Lumbricus rubellus, in a laboratory-controlled environment. Soil Biology
and Biochemistry 40:587–593.