Biology of four species of Notiphila fallén (Diptera: Ephydridae) associated with the yellow water lily, Nuphar luteum (Nymphaeaceae)

19 Pages·1997·6.9 MB·

by  L Larson

PROC. ENTOMOL. SOC. WASH.
99(3). 1997. pp. 541-559
BIOLOGY OF FOUR SPECIES OF NOTIPHILA FALLEN (DIPTERA:
EPHYDRIDAE) ASSOCIATED WITH THE YELLOW WATER LILY,
NUPHAR LUTEUM (NYMPHAEACEAE)
Len Larson and B. A. Foote
OH
Department of Biological Sciences, Kent State University, Kent, 44242, U.S.A.;
(LL) current address: Department of Natural Sciences, Shawnee State University, Ports-
OH
mouth, 45662, U.S.A.
—
Abstract: The life histories of four species of Notiphila, N. bella, N. eleomyia, N.
kentensis, and N. niidipes, that feed on anaerobic sediments surrounding roots of the
yellow waterlily, Nuphar luteiim, are described. Males of N. eleomyia and N. nudipes
form mating aggregations resembling leks on flowerbuds, flowers, fruits, and occasionally
leaves of the host plant, and mating occurs within these aggregations. Females deposit
large clusters of eggs on these plant parts, particularly the flowers and fruits. The incu-
bation period lasts 4-6 days, and newly hatched larvae drop off the egg masses and fall
into the underlying sediments where they feed during the summer and fall months. Over-
wintering occurs as nearly mature larvae. In late May and early June, larvae move to
roots of Nuphar and insert their spiracular spines into air spaces within the root tissue.
The pupal period lasts 14-22 days. Notiphila bella is univoltine, but the three otherspecies
may be bivoltine. Information is presented on the utilization ofwetland plants by different
species of Notiphila, and it is proposed that speciation and adaptive radiation involved
movement onto these different "host plants" for the purpose of obtaining oxygen by the
larvae.
Key Words: Shore flies, Notiphila, Ephydridae, Diptera, Nuphar, Ohio
Wetlands subjected to long-term inunda- modified posterior spiracles that form elon-
tion develop anaerobic conditions in the un- gate spines that can be inserted into the
derlying soils (Mitsch and Gosselink 1992). aerenchymatous tissues of plants and thus
As a result, plants and animals living in acquire oxygen (Miiller 1922; Varley 1937,
such anaerobic conditions must acquire a 1939; Keilin 1944; Hinton 1953. 1968;
A
variety of mechanisms that allow them to Hartley 1958; Houlihan 1969a, 1969b).
acquire the oxygen necessary for their met- large and widely distributed taxon having
abolic functions. Many wetland plants pos- this ability are shore flies belonging to the
sess aerenchyma in their stems, rhizomes, genus Notiphila Fallen,
and roots that allows for the diffusion or The genus Notiphila is worldwide in dis-
mass transport of oxygen from the photo- tribution, occurs in a variety of wetland
synthesizing aerial portions of the plant to habitats, and is speciose, with 53 species
the roots (Armstrong 1964, 1978; Dacey having been recorded from America north
1980, 1981; Grosse and Mevi-Schutz 1987; ofMexico (Mathis 1979, Wirth et al. 1987).
Mevi-Schutz and Grobe 1988). Larvae of Meaningful biological studies are available
some insects living in anaerobic soils have for only five of these Nearctic species, al-
542 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
though fragmentary information has been Materials and Methods
pubUshed for an additional 15. Berg (1950) Site description.—Two marshes located
reared A^. {Notiphila) loewi Cresson from in Portage County in northeastern Ohio
anaerobic soils surrounding the rhizomes (Fig. 1) were sampled in this study. The
and roots of pondweeds (Potamogeton
larger marsh is situated on the east side of
spp.). Eastin and Foote (1971) discussed the State Highway 43, 9.3 km north of the
natural history of A^. {Dichaeta) caudata northern city limits of Kent. The marsh is
Fallen, a species that is unusual within the bordered on the west by the highway, res-
genus in that its larvae are not buried in idential property on the north, and open
anaerobic sediments but crawl about on the lowland woodlands on the east and south.
surface. Larvae of this species lack spirac- The emergent marsh vegetation consists of
ular spines. Busacca and Foote (1978) pre- species of Carex, Typha, and Sparganium
sented life history observations on two spe- around the perimeter, a large stand ofTypha
cies, A^. (Agrolimna) aenigma Cresson, and and Sparganium growing intermixed on a
N. (N.) solita Walker, that obtain oxygen floating mat of dead vegetation at the east
from roots of cattails (Typha latifibula L.). end, and a large stand (ca. 2700 m-) ofyel-
They also described the eggs, larvae, and low water lily at the west end (Fig. 2). In
puparia of these two species. Deonier et al. addition to the emergent vegetation, there
(1978) described the immature stages and are thick growths of floating duckweeds,
outlined the natural history of A^. (A^.) car- Lemna minor L., Woljfia punctata Griseb.,
inata Loew, a species that is associatedwith Spirodelapolyrhiza (L.) Schleid., and water
water willow {Justicia americana (L.) milfoil, Myriophyllum exalbescens Femald.
Vahl.) growing in slow-flowing streams in The marsh is persistent and has arather sta-
southwestern Ohio and otherregions eastof ble water level. The water depth varied
the Mississippi River. from 50 to 80 cm during the two-year study
Some biological observations and indi- period.
cations of association with particular wet- The second, much smaller marsh is lo-
cated 0.8 km east of the Kent State Uni-
land plants are also available for A^. {N.)
versity main campus, between Horning
bella Loew, N. (N.) eleomyia Mathis, N.
(N.) kentensis Huryn, A^. (A^.) mathisi Hu- bRooradderaenddbUy.HS.omHiingghwRaoyad26o1n (tFhieg.we3s)t.,Irtesi-s
ryn, N. (N.) nudipes Cresson, N. (N.) pau-
idential property and a pond on the north.
roura Mathis, A^. (A^.)poliosoma Mathis, N. Highway 261 on the east, and an abandoned
(JN.) shewelli Mathis, A^. (A^.) taenia Mathis, agricultural field on the south. The vegeta-
A^. (A^.) theonae Huryn, and N. (A.) deonieri tion is more diverse than in the largermarsh
Mathis, A^. (A.) olivacea Cresson, A^. (A.) and consists of discontinuous stands of Ty-
quadrisetosa Thomson, N. (A.) scalahs pha, Carex, Phalaris, Sparganium, Eleo-
Loew and A^. (A.) scoliochaeta Mathis charis, and Nuphar. At the time this marsh
(Mathis 1979; Todd and Foote 1987; Huryn was characterized by Todd and Foote
1984, 1987). (1987), the Nuphar stand encompassed
In this paper, we present observations of some 1157 m-, but low water levels since
the natural history of Notiphila bella, N. that survey has permitted Typha to invade.
eleomyia, N. kentensis, and A^. nudipes oc- As a result, the continuous stand ofNuphar
curring in stands of the yellow water lily, in 1995 is only some 100 m-, and the water
Nuphar leuteum (L.) Sibth. and J. E. Smith. depth averages only 10 cm. —
We also discuss resource partitioning in the Sampling methods for adults. A tran-
genus Notiphila and propose a possible sect was established across the centerofthe
mode of speciation within this taxon. Nuphar stand at the Route 43 marsh (Fig.
VOLUME NUMBER
99, 3 543
OHIO
N
4
Fig. 1. Map showing locations of two study marshes in northeastern Ohio.
544 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
MARSH
#2
Figs. 2-3. 2, Map of the Route 43 marsh showing stands of vegetation. 3, Map of Horning Road marsh
showing stands ofNiiphar luteitm.
2). The transect extended south-southeast Collections of adult Notiphila were taken
from the north edge of the marsh. A rope, weekly at 2 locations in each marsh be-
m
65 long, that was attached at each end of tween early June and early October from
the transect completely crossed the width of 1991 to 1993. All collections were made
the marsh. The Nuphar stand along the during the same 24 hour period using iden-
m
transect was 45 wide. Six sampling sites tical detergent pan traps (Southwood,
m
were established along the transect at 6 1978). The pan traps consisted of white
intervals. Each site was marked by wooden polyethylene storage containers measuring
stakes that encompassed a 4 X 2 m plot. 30 X 15 X 10 cm. Each trap contained ap-
Two sampling sites were established in the proximately 50 ml of water into which one
Homing Road marsh (Fig. 3). One of these ml of dishwashing detergent had been add-
was in the center of the Nuphar stand, the ed. All traps were placed in the marshes
m
other some 5 distant where Nuphar and during the mid-afternoon and collected 24
Typha were intermixed. hours later. In the Route 43 marsh, traps
I
VOLUME 99, NUMBER 3 545
Figs. 4-5. 4, Emergence trap, cross-section diagram. 5, Diagram ofcore sampling device.
were placed at sampling sites 1 and 3, ing but prevented rainwater from flooding
whereas in the Horning Road marsh, they the trap. Traps were attached to the wooden
were placed at both collecting sites. The stakes delimiting the sample plots and the
contents of the traps were returned to the bucket part of each trap was completely
laboratory where the adult Notiphila were submerged. Each tube pan contained ap-
removed, identified, sexed, and counted. proximately 500 ml of water and one ml of
Collections of adult Notiphila from the detergent. The traps were emptied weekly
unopened buds or flowers of the Nuphar between June 15 and July 27, 192, and the
were obtained either by using a modified Notiphia identified, sexed, and count—ed.
battery-operated hand vacuum (Marshall Sampling methods for larvae. Core
1982) or by carefully placing a large poly- samples ofthe bottom substrates were taken
ethylene bag over the buds or flowers and at the sample sites in the Route 43 marsh
then breaking off the peduncle below the
on September 20, 1991 (site 1), February
water surface and sealing the bag.
18, September 25, October 8, 1992, and
During the summer of 1992, six emer-
April 6, 1993 (all six sites). Cores were ob-
gence traps were placed along the transect
tained using a 5 cm colorless, polybuterate
ionftthheeRsoaumtpel4e3pmlaotrss.h,Thoenettrraappsatweeraechceonnd- tube that was 2 m long (Fig. 5). A piston
structed by attaching a one-piece plastic fitted into the coring tube allowed the sub-
tube pan to the outside bottom of a plastic strate to be sampled without being flooded
3-gallon (11.25 L) bucket (Fig. 4). Prior to by the overlying water. Cores were placed
attaching the pan, a small hole was cut in in polyethylene bags and returned to the
the center of the bucket. A lid of clear, laboratory where they were examined for
polycarbonate plastic was attached to the Notphila larvae. Larvae were extracted
bucket with machine screws and wing nuts. from the cores either by using an elutriator
A 5 cm vent hole was cut in the center of similar to that described by Whitman et al.
the lid and covered with plastic window (1983) or adding water to the mud sample
screening. The two holes allowed for vent- to reduce it to a slurry that was then spread
—
546 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON I
over the bottom of a large tray and inspect- Table 1. Temporal distribution ofadults ofall spe-
ed visually. — cies ofNotiphila collected in two marshes in Portage
County, Ohio.
Rearing methods. Portions of Nuphar
rhizomes and attached roots were removed
from the marsh substrate at various times Week
throughout the year and examined visually
in the laboratory for attached larvae and/or
puparia. Puparia were carefully removed
from the roots and placed on moist sphag-
num moss in test tubes (Berg 1950). They
were oriented in the moss so that the pos-
terior spiracular spines of the puparia were
exposed to air. No attempt was made to rear
larvae. —
Identification of adults. Males were de-
termined by using keys of Mathis (1979)
and Huryn (1987). Tentatively determined
specimens of each species were submitted
to Wayne Mathis at the Smithsonian Insti-
tution for confirmation.
Results of Trapping in the Two
Marshes
Pan trapping in the Route 43 marsh.
Approximately 53,200 adult Notiphila of
eight species (Table 1, Fig. 6) were ob-
tained in the detergent pan traps during the
three-year survey. Ofthese, 10,620 (20.4%)
were males. Three species, TV. eleomyia, N.
kentesis, and N. nudipes dominated
throughout the study (Figs. 7-9), represent-
ing 95.2% of the total number collected.
These three, plus N. bella, constituted over
97% of the males collected. N. eleomyia
was the most abundant species, accounting
for 60.3% of the total number The second
most abundant species was A^. kentensis, ac-
counting for 25.5% of the males collected,
whereas A^. nudipes accounted for only
9.4% of the males identified. Notiphila bel-
la was present only during late spring and
early summer and commonly was the first
species to emerge (Fig. 10). Four other spe-
cies, N. olivacea, N. pauroura Mathis, N.
solita, and N. taenia, were only collected
sporadically. Notiphila taenia was taken
predominantly from mid to late June, al-
though a few were taken as late as October.
VOLUME 99. NUMBER 3 547
lOOOOrr
IOOO1
CO
yj
-J
LL
O
10O1
a:
LU
QQ
I3E
10=
eleomyiakentensis nudipes bella pauroura taenia olivacea solita
NOTIPHILA SPECIES
Fig. 6. Total number ofNotiphila males collected in the Route 43 marsh during 1992.
within days of the same date on all three emergence traps. All appeared between
years, VI-19-91, VI-17-92, and VI-16-93. VI-17 and VI-29-92. Most of the adults
Pan trapping in the Horning Road were taken at site 1, and none was taken in
marsh.—Only 408 adults (38.2% males) of the trap at site 4. —
five species of Notiphila were taken in the Core sampling. Twenty Notiphila lar-
Homing Rd. marsh during the year-long vae, all third instar, were extracted from the
survey (Table 1). The relative abundances core samples of mud that were taken inter-
of the five species were somewhat different mittently in the marshes (Table 2). No lar-
than those obtained in the larger marsh. A^o- vae where reared to the adult stage, so spe-
tiphila eleomyia and N. kentensis accounted cies identification was not possi—ble.
for 51.9% and 20.5%, respectively, of the Rhizome and root sampling. A total of
adults trapped. However, the third most 229 larvae and 91 puparia were collected
abundant species was N. pauroura, ac- from samples ofNupharrhizomes androots
counting for 13.5%, followed by N. nudipes (Table 3). All ofthe larvae were found dur-
(11.5%) and N. oliva—cea (2.6%). ing the late fall and early spring months in
Emergence traps. Somewhat surpris- mud adhering to the rhizomes and roots. In
ingly, only nine males and 15 females of contrast, all puparia were firmly affixed to
three species, N. eleomyia (5), N. nudipes the primary roots ofthe rhizomes and roots
(3), and A^. bella (1), were collected in the (Fig. 21) and were found only during late
J
PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
548
800-
700-
600-
500-
400-
U-j 300-
<
^
200- ' :
100-
J ^ I J J J J
a. I
19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 35 36 37 38 39 40
WEEK OF THE YEAR
^g
1991 1992 1993
450-
400-
350-
300-
250-
200-
fl-R
LU 150 M
_<l
10O
50
»
la ^ ^
I
19 20 21 22 23242526 2728 2930 31 33 3435 3637 38 39 40
WEEK OF THE YEAR
H ^
1991 1992 1993
8
Figs. 7-8. 7, Seasonal distribution ofNotiphila eleomyia in the Route 43 marsh. 8, Seasonal distribution of
N. kentensis in Route 43 marsh.
I
VOLUME NUMBER
99, 3 549
200-
160-
120-
804
UJ
<
A0-\
J J J ^ J _
-
19 20 21 22 2324 2526 2728 2930 31 32 3335 3637 38 39 40
WEEK OF THE YEAR
1991 Hi ^^^^ ^S 13^3
j
80
70-
60-1
50
LU
CO
Zl 40-1
HI
^
30-1
20-
10-
19 20 21 '22'23'24'25'26'27'28'29'30'3l'32'33'35'36'37'38'39'40
WEEK OF THE YEAR
^
^1991
1992 1993
10
Figs. 9-10. 9, Seasonal distribution of adult Notiphila nudipes in the Route 43 marsh. 10, Seasonal distri-
bution ofadult Notiphila bella in the Route 43 marsh.
550 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
W
UJ
—I
U-
UL
o
cc
LU
QQ
IDE
Z
eleomyia kentensis nudipes bella pauroura taenia oiivacea solita
SPECIES OF NOTIPHILA
EDGE CENTER
11
30
PeakIsthemaximumnumberofNoUphllacollectedIna24hour 27275(06/26-06/30)
period,bothpantraps.
1991 1992 1993
YEAR
^PEAK
TOTAL
12
Figs. 11-12. 11, Spatial distribution ofadultNotiphila in the Route43 marshduring 1992. 12, Total number
ofNotiphila collected in the Route 43 marsh between 1991 and 1993.