Parvidrilus Strayeri, A New Genus And Species, An Enigmatic Interstitial Clitellate From Underground Waters In Alabama

11 Pages·1999·5.5 MB·

by  C Erseus

PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
I12(2):327-337. 1999.
Parvidrilus strayeri^ a new genus and species, an enigmatic interstitial
clitellate from underground waters in Alabama
Christer Erseus
Department of Invertebrate Zoology, Swedish Museum of Natural History,
Box 50007, SE-I04 05 Stockholm, Sweden
—
Abstract. An exceedingly small oligochaete, Parvidrilus strayeri, a new
genus and species, is described from a streambed in northern Alabama, U.S.A.
mm
The species is up to 1.4 long (with up to 33 segments) and has several
unusual features. In ovigerous specimens, a clitellum is developed as a pair of
lateral rows of a few, large, swollen epidermal cells in segments (IX-) X-XII
(-XIII, -XIV). Chaetae are absent from segment II. Otherwise, in the anterior
part of the body, there are long hair chaetae as well as small crotchet chaetae
in both dorsal and ventral bundles. Furthermore, the chaetal bundles are situated
posteriorly in each segment. It is unclear whether gonads are paired or un-
paired; testes (testis?) are in segment XI, ovaries (ovary?) in XII. The other
reproductive organs include a U-shaped muscular 'genital body' in segment
XII and a V-shaped 'copulatory organ' in segments XII-XIII; the exact nature
and function of these structures are unknown. The genus is proposed to be
classified as the single member of Parvidrilidae, new family. It appears to be
most closely related to two, largely Southern Hemisphere, aquatic clitellate
A
families, Capilloventridae and Phreodrilidae. possible relationship to the
monotypic, South American taxon, Narapidae, is also discussed.
In the course of a study of the under- stained with Rose Bengal, sorted under a
ground fauna of a crystal clear, spring fed dissecting microscope, and stored in 70%
stream in Alabama (Strayer et al. 1995), ethanol. The material was then sent to the
specimens of an exceedingly small, undes- present author, who stained several individ-
cribed, oligochaete were encountered. Dr. uals in alcoholic paracarmine and mounted
David L. Strayer (Institute of Ecosystem them whole in Canada balsam on micro-
Studies, Millbrook, New York, U.S.A.) scope slides. Most of the measurements in
placed the material at the present author's the description refer to this whole-mounted
disposal. It is described as the type species material, examined under a light micro-
of a new genus, Parvidrilus, in the present scope. Due to the small dimensions, how-
paper. The phylogenetic affinities of the ever, the details of the chaetae could not be
new species, which appears to represent a observed even when using a high-resolution
new higher level taxon of the Clitellata, are lOOX oil immersion lens. Therefore, exter-
also discussed. nal traits were also investigated by means
of scanning electron microscopy. Since the
Material and Methods animals were too small for the perforated
containers available for critical point dry-
The worms were collected at a single site ing, they were simply dehydrated in 99%
in Hendrick Mill Branch, northern Ala- ethanol, transferred to butyl acetate, and air-
bama, in October 1990 (Strayer et al. 1995). dried. This is a rough method, but thanks
They were fixed in buffered formalin. to their sturdy cuticle and small size the
328 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
—
worms maintained the body shape accept- Type species. Parvidrilus strayeri, new
ably, at least in a comparison with individ- species.
—
uals prepared for light microscopy. Three Other species. None.
specimens were mounted on double-sided
tape, coated with gold and examined with Parvidrilus strayeri, new species
SEM.
Figs 1—2
The holotype and some paratypes of the
new species, Parvidriliis strayeri, are de- Ohgochaeta n. sp.: Strayer et al. 1995:506.
posited in the National Museum of Natural
History (USNM), Smithsonian Institution, Holotype.—VS'^M 185769, whole-
mounted specimen.
Washington, D.C., additional paratypes in —
the Swedish Museum of Natural History Type locality. ^A hyporheic site in a sand-
(SMNH), Stockholm. gravel bar, in Hendrick Mill Branch, a spring-
fed stream about 20 km NE of Pinson,
ParvidriUdae, new family Blount Co., Alabama, U.S.A., 33°52'12''N,
— 86°33'57'W, 4 Oct 1990, coll. D. L. Strayer.
Etymology. ^Family name (-idae) based At this site, the stream is 3—6 m wide and
on Parvidrilu—s, new genus (type genus). runs through a hardwood forest in a lime-
Diagnosis. Until additional species are stone terrain. The bottom varies from sand
found, the new family is characterized by to exposed bedrock, with a predominance
the features of the type species of the type of coarse sand, angular gravel and small
genus. They can be summarized as follows: (10-15 cm) stones. Generally the alluvium
Meiofaunal freshwater oligochaetes,
is thin, but a large deposit of sand and grav-
mm
about 1 long. Chaetal bundles situated el is held in place by a dam about 3 m high.
posterioriy in each segment, but completely At the time of collection, the emergent part
absent from segment 11. In anterior part of of this deposit was 3-4 m wide, about 30
body, both dorsal and ventral bundles with m m
long, and reached about 0.5 above the
very long hair chaetae as well as short stream water level. Because the dam leaked
crotchet chaetae; dorsal crotchets single- from the base, water flowed down into and
pointed, ventral ones bifid. In posterior part through the bar. Subsamples were taken
of body, dorsal bundles similar to anterior
from 16 wells in the bar, using a Bou-
dorsal ones, ventral bundles with bifid Rouch pump (Bou 1974), all wells yielded
crotchets only. In ovigerous specimens, cH-
water freely. Dissolved oxygen was 0-8.0
tellum developed as a pair of lateral rows ppm, with most readings 2-6 ppm. Other
of large, swollen, transparent, cells in seg-
chemical characteristics (means of several
ments (IX-) X-Xn (-Xm, -XIV). Ahmen- subsamples): Ca 22.2 ppm; Mg 11.6 ppm;
tary canal simple, without diverticula. It is K 0.5 ppm; Na 0.7 ppm; NO3 0.9 ppm; SO4
unclear whether gonads are paired or un-
1.8 ppm; CI 1.2 ppm; Dissolved Organic
paired; testes (testis?) in segment XI, ova- Carbon (DOC) 0.5 ppm (Strayer et al. 1995;
ries (ovary?) in XII. Reproductive organs
Strayer, pers. comm.).
complex, including U-shaped muscular US^M
Paratypes.— 185770-185776-
'genital body' in XII and V-shaped 'copu-
000000, seven whole-mounted specimens;
Xn-Xm.
latory organ' in SMNH
Type coU. 5085-5092, eight whole-
SMNH
mounted specimens; Type coll.
Parvidrilus, new genus SEM
5093, three specimens mounted on a
—
A
Etymology^ combination of parvus stub; all from—type locaHty.
(Latin for 'smaU') and drilus (Greek for Etymology. Named for Dr. David L.
'worm'). Strayer, who collected the material and was
—
Diagnosis. As for family. the first to reaUze that the species was a
VOLUME NUMBER
112, 2 329
Fig. 1. Parvidrilus strayeri, new genus and species; SEM micrographs. A, postclitellar part of body, showing
dorsal hair chaetae (he) ventral bifid chaetae (in bottom part of figure), and intersegmental fiirrows (if); note the
posterior location ofbundles in the segments; B, anterior end ofbody showing mouth (m), achaetous segment 11 (II),
and dorsal (top of figure) and ventral chaetae (middle and bottom of figure) of segments III-V; C, bundle of ventral
chaetae of segment EX, showing hair chaeta (he) and bifid crotchets (be); D, bundle of dorsal chaetae of segment X,
showing hairchaeta (he), and single-pointed crotchets (sc); note also thin outerpart ofhairchaetae ofanothersegment;
E, bundle of ventral chaetae of postclitellar segment, showing two bifid crotchets; F, ventral view of genital bursa
(bu) in segment XII, showing lateral bulbous swellings (bs), posterior triangular lappet (tl). and ventral chaetae (vc).
330 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
Fig. 2. Parxidrilus strayeri, new genus and species. A, schematical, horizontal view of segments XII and
Xm, showing general outline of 'genital body' and 'copulatory organ'; B, somewhathorizontal view ofsegments
Xl-Xni of one paratype: C, somewhat lateral view of segments XI-XIII of another paratvpe. Abbreviations: bs,
bulbous swelling (of body wall); bu. location of genital bursa (cf. Fig. IF); c. chaeta; cc. clitellar cell; co.
copulatory organ; gb, genital body; ov, ovary; pe, penis/pseudopenis; ps, penial/pseudopenial sac; sf, sperm
funnel, t. testis.
VOLUME NUMBER
1 12, 2 331
new taxon of considerable systematic inter- thick, with upper tooth thinner and shorter
est. — than lower tooth. Within these bundles, up-
Description. Length (five complete permost (most lateral) chaeta bifid, fol-
specimens) 0.7-1.4 mm, 18-33 segments. lowed by a hair, and these two chaetae
Width at genital region 0.03-0.10 mm. Pro- clearly separated from two, more ventral,
stomium rounded, somewhat narrower than bifids (Fig. IC). Postclitellar ventral bun-
and well set off from peristomium; prosto- dles with two to three bifid crotchets (Fig.
mial epidermis with numerous (stained) cell IE), similar to anterior ventral bifids. Mod-
nuclei, probably indicating a glandular or ified genital chaetae absent.
sensory function. Posterior part of body Ventrally in segment XII, body wall
(Fig. lA) more clearly annulated (i.e., with forming a conspicuous, generally somewhat
distinct intersegmental furrows; Fig. lA, if) "X"-shaped genital bursa (Fig. IF); im-
than anterior part. Pygidium generally de- pression of an X facilitated by a pair of
marcated, somewhat narrower than last large, bulbous, swellings (Fig. IF, bs), one
(true) segment. Cuticle smooth, but foreign at each side of bursal opening, and an in-
particles often adhering to it here and there distinct, mid-ventral, triangular lappet (Fig.
along body of worm. Clitellum poorly de-
IF, tl), located immediately posterior to bur-
veloped in most individuals; but in oviger-
sal opening.
ous specimens, a row of large, swollen, Spermathecal openings not observed.
transparent, epidermal cells (Fig. 2B, cc) Brain located within, and with front end
present on each side of worm in segments
reaching anterior coelomic lining of, peris-
(IX-) X-XII (-Xni, -XIV).
tomium. Nerve cord ventral, of normal mi-
Chaetal bundles situated posteriorly in
crodrile oligochaete appearance. Alimenta-
each segment (Fig. lA), but lacking com-
ry system of normal microdrile oligochaete
pletely in segment II (Fig. IB). Anterior
type too: simple pharynx with dorsal pha-
dorsal bundles each with one to two (oc-
ryngeal bulb, somewhat sinuous esophagus
casionally three) long, whip-Uke, hair chae-
with a few pharyngeal (?) gland cells scat-
tae (Fig. ID, he), alternating with two or
tered in segments V-VIII, followed by a
three (occasionally four) single-pointed,
narrow, simple intestine; no particular en-
smaller crotchet chaetae (Fig. ID, sc); hairs
largements or diverticula on gut. Large, dif-
occasionally up to about 200 |xm long (ex-
fuse cells of chloragogen tissue present
act length difficult to measure due to strong
along most of gut. Free coelomocytes not
curvature of hairs and poorly resolved view
observed.
of tips), entaUy about 1 jjim wide, progres-
In three specimens, a small lump of cells
sively tapering and only about 0.1 ixm wide
at ectal end; crotchets 15—25 ixm long, in anterior end of coelom of segment XI
about 0.5-0.6 (xm thick, with somewhat probably an (unpaired?) testis (Fig. 2C, t?);
blunt tips. Postclitellar dorsal bundles each in another worm, a single sperm bundle
with one or no hair chaeta (Fig. lA, he) and present in coelom of this segment; other-
two single-pointed crotchets. In anterior wise male gonads or developing spermato-
segments (at least in III-VII, but generally zoa not observed. In nine specimens, an
also including a few additional pre-genital ovary (apparently developed on one side
segments, and sometimes even as far back only) observed in anterior part of segment
as in XV), ventral bundles each with one XII (Fig. 2B, C, ov); three of these worms
hair chaeta (Fig. IC, he), and three (occa- ovigerous, i.e., with a large mature Qgg fill-
sionally four) bifid crotchets (Fig. IC, be); ing whole width of coelom, and extending
ventral hairs slightly shorter and thinner through one or two segments, in region of
than corresponding dorsal hairs; bifids XIII-XV In two specimens (only), a sperm
about 20-25 |jLm long, about 0.9-1.4 |ULm funnel discernible at anterior side of septum
332 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
between XI and XII (Fig. 2B, C, sf), but its jjim long, 10-21 ixm wide, with thick, mus-
continuation into a vas deferens not seen. cular, wall, and containing a coiled, slender
Other internal genitalia (in XII-XIII) tube. In one damaged specimen, tubes
complex (Fig. 2), but due to quality of fix- squashed out from sacs, appearing as long
ation and small dimensions difficult to in- penes (Fig. 2C, pe), but it appears as if tips
terpret using conventional oligochaete ter- of these are normally located inside inner
minology. Two conspicuous structures pres- ends of sacs rather than at mid-ventral at-
ent, here referred to as the 'genital body' tachment point in body wall. It is thus un-
and the 'copulatory organ', respectively. known whether tubes are protrusible (i.e.,
Genital body (Fig. 2A-C, gb) a "U"- penes) or eversible structures (i.e., pseudo-
shaped structure incorporated in ventral penes).
—
body wall in segment XII; the two arms Remarks. Although there is a possibil-
forcing body to bulge considerably, corre- ity that the genital body in segment XII is
sponding to two bulbous swellings at lateral used for storing sperm from a concopulant
sides of genital bursa (Fig. IF, bs). Arms of (see above), typical spermathecae were not
genital body more or less oval, 20-35 ixm observed.
long, 15-23 |xm wide, oriented along long Several points in this description need to
axis of worm, and united anteriorly. At ear- be clarified by future studies. Nevertheless,
ly developmental stages, lobes appear to Parvidrilus strayeri is easily separated from
contain a lumen. At full maturity, wall of all other known oligochaete taxa. See Dis-
genital body thick, heavily muscular and cussion below.
—
folded in complex manner (Fig. 2B, C, gb), Distribution and habitat. Known only
with indistinct lumen (lumina?); sometimes from the type locality in Alabama, USA.
densely packed cilia (see Fig. 2B) and/or Interstitial groundwater.
spermatozoa (?) visible inside. At late stag-
es of development, lobes tend to break up Discussion
into a number of secondary, pear-to-spin-
dle-shaped, packages of muscle fibers (as in Parvidrilus strayeri is clearly a clitellate.
Fig. 2B). Function of genital body un- It appears to be hermaphroditic (the geni-
known; possibly having something to do talia of all specimens look the same) with
with storage and/or ejaculation of sperm, ei- gonads in specific segments, and it has an
ther before (an atrium?) or after copulation eversible, thickened, pharynx roof, a brain
(a spermatheca?). Whether genital body has located behind the prostomium, and large
any permanent or temporary opening to the glandular epidermal cells in the genital re-
exterior or any connection with the sperm gion suggesting the existence of a clitellum
funnels or copulatory organ unknown. (see Purschke et al. 1993). In a traditional
Copulatory organ (Fig. 2A, co) bilobed, sense, the worm is a member of the Oli-
somewhat "V"-shaped, consisting of a pair gochaeta; but there is now increasing evi-
of straight or somewhat curved sacs (Fig. dence that this taxon is paraphyletic unless
2B, C, ps), conrununicating with each other leeches and leech-like groups are included
mid-ventrally in most posterior part of seg- (Purschke et al. 1993, Brinkhurst 1994, Sid-
& &
ment XIL At point of union of the two sacs, dall Burreson 1996, Ferraguti Erseus
A
copulatory organ appears anchored in the 1999). formal phylogenetic analysis to
ventral body wall, in a position correspond- establish the more specific systematic po-
ing to apex of the mid-ventral, triangular, sition of Parvidrilus within the Clitellata, is
lappet located in posterior wall of genital not meaningful until some uncertainties in
bursa (Fig. IF, tl; see above). Inner ends of the description have been clarified. As there
sacs extending obliquely and freely back- is yet no strong indication as to which cli-
wards into coelom of XIII. Each sac 25-60 tellate subgroup the new species belongs.
VOLUME NUMBER
112, 2 333
outgroups for such an analysis would need Hemisphere (although a few phreodrilids
to be selected from outside the Clitellata, occur north of the equator), but a further
implying that most ingroup and outgroup comparison with them is pertinent here as
character states would not be comparable. both (see Harman & Loden 1984; Erseus
In some ways, however, the new species 1993; Pinder & Brinkhurst 1997a, 1997b)
is unusual and unique (see Table I). First, it are characterized by absence of chaetae in
is one of the smallest clitellates known. segment II (for phreodrilids, at least with
mm &
With a body length of about 1 it resem- regard to the dorsal chaetae; Pinder
bles only the smallest Chaetogaster spp. Brinkhurst 1997a), and presence of hair
(Naididae) (see Sperber 1948), an undes- chaetae in the other segments, i.e., two
cribed freshwater species tentatively as- striking similarities with the chaetal pattern
signed to Capilloventer (Capilloventridae) in Parvidrilus (Table I).
&
from Western Australia (Pinder Brink- The additional feature of ventral hair
hurst 1997b); and a miniature terrestrial chaetae is, within the CHtellata, shared only
species of Enchytraeidae from Italy, Mar- by Parvidrilus and Capilloventridae and
ionina eleonorae Rota, 1995. Some marine may be homologous. However, Capilloven-
&
oligochaetes are just slightly longer. Ex- tridae, as currently defined (Pinder
mm
amples within the 1.5-2.5 range are nu- Brinkhurst 1997b), is characterized by
merous species of the subfamily Phallodri- modified hair-like genital chaetae, sperma-
linae (Tubificidae; see, e.g., Erseus 1980, thecae in segment Vn, and a pair of blind
1989, 1990, 1992), and Randiella caribaea ventral sacs (salivary glands?) opening into
&
Erseus Strehlow, 1986 and R. minuta Er- the mouth cavity (the two first features also
seus & Strehlow, 1986 (Randiellidae; see known from the Randiellidae; see Erseus
Erseus & Strehlow 1986, Erseus 1997). To and Strehlow 1986). As none of these is
my knowledge, there is no freshwater tu- present in Parvidrilus, inclusion of the new
mm
bificid that is even close to the 0.7-1.4 genus in Capilloventridae would imply re-
range that characterizes Parvidrilus. ductions of all three traits, which is a less
Second, in Parvidrilus strayeri, the four parsimonious hypothesis than to regard
chaetal bundles of each segment are located Parvidrilus as a taxon outside Capilloven-
in a more posterior position within the seg- tridae. Moreover, in Capilloventridae but
ment than in other oligochaetes. Third, the not in Parvidrilus, the chaetal bundles of
clitellar cells are large in relation to the each side are located close together and
body diameter, few in number, and restrict- widely separated from those of the other
ed to two lateral rows, one at each side, side, somewhat like the distribution of
through a few segments of the worm. These chaetae on parapodia of polychaetes (Er-
features are likely to be autapomorphies of seus 1993). This could be a plesiomorphic
Parvidrilus or of a group including as yet condition reflecting ancestry of the Clitel-
unknown taxa. lata among the polychaetes (cf. Westheide
Although complete male ducts have not 1997), and in which case the Capilloventri-
been observed in Parvidrilus, the position dae could be the most ancestral group of all
of the genital bursa indicates that male Clitellata; alternatively, it is an additional
pores (or an unpaired male pore?) are pres- autapomorphy of Capilloventridae.
ent in segment XII. In this respect the new The Phreodrilidae comprises a total of
taxon bears resemblance to four other mi- about 60 species with great morphological
crodrile families, Enchytraeidae, Propappi- variation with regard to chaetae as well as
&
dae, Capilloventridae and Phreodrilidae, genital organs (Pinder Brinkhurst 1997a).
and a few representatives of the Lumbri- In phreodrilids, the dorsal chaetal bundles
culidae. Capilloventridae and Phreodrilidae frequently consist of long hair-like chaetae
are regarded as endemic to the Southern accompanied by short, single-pointed, "lat-
V ' I
334 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
.cy« du)
3
60
_^ u<u1J
c;S
^ -i-i ^
^<1) cSd ac2C ^(li tco-«l Xc()dU Xo&)0
-0Xt-)i <o-> E t+D-i- « Iu2-" >Ui Tcc3
^_(cU £-3a i0n01 C(1) C(y<O1Uj)h _c ^ TO13/1 3O X3) XCct)/33 !0S0 33 >C< _Xc XcCci/33
^
(U a
C/1
3
o
-^
>>
C>0 "oT /— 'u' 'oT ^(UV 'oT ^ TO3
.')s„-H] j(n=1) Xoc)d Xoc)« XOc)3 Xoe)« XCcJJd Xoc)« Xoc)« X(3)30
^(c-U3H x(:i; S 3 Cac3x aaex caa3 caD«h Csald- aDah rDDt,h '3•3 _^
cd j= •n ^ O io-t o to-i o o O
ii ^ I X) c 3 c 3 C S c c -S
o
CC/)
u o
-w
I3T| •r'
^ rrl
Oh
ci-«i fO= ^C_, c o3 T3
r XC)/5 4^c-d1 uC/5 "O -3*— XOI
c« aDh (UDUih (3U cv3: a3o
So 5o s s^. ^1/3 <4-i 'Doh X3) 3 ^
o c •f^ T3 13 C3f* 1 2 -3!-> =5 KX KX 3
y) e "ob Dh g ^
a ty5 •OT3 '35 X5 S .S -S -S
T3
««
D S 4J ^i?3^3s X•1O;i_^! o
'J>a o^ <u ->BB^n1 .D1c/^3- X(30-)31 1^Mc3 ^"(Mo(o5U0 T-1to>3a3a3/3 T"_'c3aH3/313o X30O;D3i-3!, H13D-^h7-h X033of3ic0 .tX33t .I>33t'Ha«s-^.i
Si cd
(U "^ ^<u
3
fe
- ^ Ou
.a T3 Dh
o5b .3-^e g^ Dh d1>^ TS33
" UO4 c3d aO -3t-i
-a _g c1r1La/))1 X-u<Cc13/-udl1 fOLcol/h)1J 13 cnC/33 (3<5u0 X) Xcid CTN, .1IC—b^ XccC)/d3 Xc3C)d«
o o
^ ic3 *"
o -
-S X3
o
e? Dh
(U
(U c3 c DC3 O Xey!d xo; d3
3 k3 U 1/5
XI
(rUj c/3 u OXua 0) (oooc^ S 1T333 XSrcIia3 •-oU43—1 cd xc:d ^ j^'"8g °^D§3h X^e^I 1X233)
HOT ^ aNi" Uxc:d U c/1 U2 c« c3 QO O3 > •^ i ^Eh 3^
c/3 DC
VOLUME 112, NUMBER 2 335
eral support chaetae", an arrangement sim- ital system in a more anterior position (Ta-
ilar to that found in Parvidrilus strayeri ble I), Narapa has a male gonoduct (in seg-
&
(but also similar to the dorsal 'hairs and ment VI) (Righi Varela 1983:figs 4-6)
needles' in species of Naididae and Opis- with an outline comparable to one possible
tocystidae). The crucial point would then be interpretation of the reproductive system in
to what extent the curious genital body and Parvidrilus. In Narapa, the sperm funnel is
copulatory organ of the new species are ho- followed by a short vas deferens (not yet
mologous to phreodrilid genital structures. observed in Parvidrilus), leading to a ven-
They show some superficial resemblance to tral glandular, tubular atrium (possibly cor-
the atria and eversible pseudopenes, respec- responding to a lateral arm of the 'genital
tively, of the species of Phreodrilus Bed- body' in Parvidrilus), followed by a pos-
&
dard (see Pinder Brinkhurst 1997a), al- teriorly bent-over penial sac with a winding
though in Parvidrilus the two kinds of lumen (possibly corresponding to a copu-
structures do not appear to be continuous latory sac in Parvidrilus). It is also note-
with each other as the atria and pseudope- worthy that the ovary (in VII) is reported
nes are in Phreodrilus. Moreover, the to be unpaired in Narapa', in none of the
phreodrilid atria are filiform invaginations, specimens of Parvidrilus strayeri was more
lying freely in the coleomic cavity, whereas than one ovary observed. It is an open
the Parvidrilus genital body is in very close question whether these similarities are syn-
contact with (merely as a pair of swellings apomorphic or convergent, but Narapidae
of) the body wall. There are also other dif- and Parvidrilidae are both monotypic and
ferences between Phreodrilidae and Parvi- each possesses its own autapomorphies (Ta-
drilus (Table I). In phreodrilids, the general ble I). As currently defined, they can, there-
body size is one order of magnitude larger fore, at most be regarded as sister taxa.
than that of Parvidrilus, the ventral chaetae However, relevant comparisons with oth-
are consistently paired, there is a thin cli- er aquatic microdrile taxa have still not
tellum of normal microdrile type and it is been exhausted. For instance, it could be
generally restricted to segments XII-XIII, suggested that the U-shaped genital body of
there are spermathecae in segment XIII, and Parvidrilus strayeri is a derivative of a pair
if hairs are present, the lateral support chae- of atria of the kind found in the family Tub-
tae do not usually project from the chaetal ificidae, and that its position in segment XII
sacs. Many ofthese features are shared with is merely an autapomorphic rearward shift
other aquatic clitellate taxa, but the lateral of a tubificid male system. Following this
support chaetae, the position of the sper- line of reasoning, the copulatory organ of
mathecae (in segment XIII), and the well Parvidrilus (Fig. 2C) could be interpreted
developed tubular atria mentioned above, as an indication of a close relationship with,
&
are likely to be autapomorphies supporting e.g., Teneridrilusflexus Erseus Hiltunen,
monophyly of the Phreodrilidae. Thus, it 1990 (in Erseus et al. 1990). The latter is a
does not appear appropriate to place Par- North American Great Lakes freshwater tu-
&
vidrilus in the Phreodrilidae. bificid (reported also by Stacey Hubley
&
Narapa bonettoi Righi Varela, 1983, 1994), with small, convoluted, tubular pe-
the single representative of the family Nar- nial organs contained within muscular sacs
apidae and known only from the Parana (Erseus et al. 1990:fig. 2D, E). However,
&
River in Argentina (Righi Varela 1983, these similarities are probably coincident
Brinkhurst & Marchese 1989), is another and convergent. As noted above, the chaetal
aquatic oligochaete taxon with an unclear pattern and the segmental position of the
systematic position. It shows some curious genitalia strongly suggest that Parvidrilus is
resemblance to Parvidrilus. Although lack- more closely related to the Capilloventridae
ing chaetae completely and having its gen- and Phreodrilidae than to the Tubificidae
—
336 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
(Table I). Furthermore, the tubificid atria probably not a rare animal, once the right
extend freely into the coelom, rather than habitats are searched.
being incorporated in the body wall as is Parvidrilus strayeri deserves further at-
the case with the genital body of Parvidri- tention. New material needs to be studied
lus. by methods that would enable a detailed
To conclude, it seems justified to estab- scrutiny of the true nature of its miniature
lish a higher level taxon, Parvidrilidae, new genital organs, which may throw additional
family, for Parvidrilus on the basis of the light on its systematic position. Molecular
available morphological evidence. This systematic analyses of this enigmatic taxon
classification is not likely to render any of may contribute towards the same end.
the other clitellate families paraphyletic.
Several features of Parvidrilus/^2cr\idu\i- Acknowledgments
dae are probably autapomorphic: the ex-
treme miniaturization, the chaetal bundles I am indebted to Dr. David L. Strayer, for
situated posteriorly in each segment, the cli- generously placing the material at my dis-
tellum modified into two lateral rows of a posal, and for sharing published and un-
few large glandular cells, and the unique, published information; to Dr. Anders Waren
(SMNH) for invaluable assistance with
complex, genital organs surrounding a con-
spicuous mid-ventral bursa in segment XII. scanning electron microscopy; to Ms. Bar-
bro Lofnertz (University of Goteborg), Mrs.
In its area of distribution, Parvidrilus is
Anna Hedstrom and Ms. Christine Hammar
part of a particular association of inverte-
brates ('stygobionts') adapted to life in in- (both SMNH), for technical assistance; to
terstitial groundwater, an association which Dr. Ralph O. Brinkhurst (Hermitage, TN,
also includes the polychaete Troglochaetus USA) and Dr. Kathryn A. Coates (Bermuda
sp., aeolosomatids (Annelida, Aphanoneu- Biological Station for Research, Inc), for
ra), smaller lumbriculid (e.g., Stylodrilus constructive criticism of the text; and the
wahkeenensis Rodriguez & Coates, 1996) Swedish Natural Science Research Council,
and naidid oligochaetes, bathynellacean for financial support.
crustaceans, microcerberid isopods and nu-
merous benthic cyclopoid copepods (Rod- Literature Cited
&
riguez Coates 1996, Strayer et al. 1995,
& Bou, C. 1974. Les methodes de recolte dans les eaux
Strayer Reid in preparation, Reid et al. —
souterraines interstitielles. Annals de Speleo-
in preparation). Although still greatly over- logie 29:611-619.
looked, this rich stygobiont fauna appears Brinkhurst, R. O. 1994. Evolutionary relationships
—
to characterize a vast area of unglaciated within the Clitellata: an update. Megadrilogi-
ancient terrain in eastern North America. ca 5:109-116.
Some authors (e.g., Wagele et al. 1995, , & M. Marchese. 1989. Guide to the fresh-
water aquatic Oligochaeta of South and Central
Reid 1998) have already pointed out that America.—Coleccion CLIMAX No. 6. Asocia-
many endemic interstitial microcrustaceans cion Ciencias Naturales del Litoral, Santo
of this region appear to represent an old Tome, Argentina, 179 pp.
continental fauna, with closely related, but Erseus, C. 1980. Taxonomic studies on the marine gen-
era Aktedrilus Knollner and Bacescuella Hrabe
anatomically distinct Eurasian counterparts.
(Oligochaeta, Tubificidae), with description of
—
It is possible that Parvidrilus is a northern seven new species. Zoologica Scripta 9:97—
representative of a group of aquatic cHtel- 111.
lates, which also contains the Southern . 1989. Marine Tubificidae (Oligochaeta) ofthe
Hemisphere families, Capilloventridae, Arabian Gulf coast of Saudi Arabia, part 5.
Fauna of Saudi Arabia 10:11-19.
Phreodrilidae and, possibly also, Narapidae.
1990. Marine Oligochaeta ofHong Kong. Pp.
Parvidrilus was common at Hendrick 2.59-335 in B. Morton, ed.. Proceedings of the
MiU (D. L. Strayer, pers. comm.) and is Second International Marine Biological Work-