December 2002
Notes
605
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FIG. 1-Podostemon ceratophyllumgrowing epizoically on Actinonaias ligamentina. Photo by Caryn Vaughn.
Virginia. American Journal of Botany 71:130136.
NELSON,E. N., AND R. W. COUCH. 1985. Aquatic
plants of Oklahoma I: submersed, floatingleaved, and selected emergent macrophytes. Oral
Roberts University, Tulsa, Oklahoma.
C. T., ANDG. E. CROW.1983. Distribution
PHILBRICK,
of Podostemum ceratophyllumMichx. (Podostemaceae). Rhodora 85:325-341.
REPRODUCTION
BY YOUNG-OF-YEAR
ITS IMPLICATIONS
C. T., ANDA. NOVELOR. 1995. New World
PHILBRICK,
Podostemaceae:
ecological and evolutionary
enigmas. Brittonia 47:210-222.
2001. The
VAUGHN,C. C., AND C. C. HAKENKAMP.
functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology 46:1431-1446.
Submitted5 September2001. Accepted29January 2002.
AssociateEditor was Steven Goldsmith.
RED SHINER (CYPRINELLA LUTRENSIS) AND
FOR INVASION SUCCESS
EDIE MARSH-MATTHEWS,*WILLIAMJ. MATTHEWS,KEITH B. GIDO, AND REBECCAL. MARSH
Sam Noble OklahomaMuseum of Natural History and Departmentof Zoology,Universityof Oklahoma,
Norman, OK 73072 (EMM, KBG)
Sam Noble OklahomaMuseum of Natural History and Biological Station, Universityof Oklahoma,
Norman, OK 73072 (WJM)
Norman High School, Norman, 'OK 73069 (RLM)
Present address of KBG:Division of Biology,AckertHall, Kansas State University,Manhattan, KS 66506
*Correspondent:emarsh@ou.edu
Cyprinella lutrensis (red shiner) is one of the
most widespread
and abundant minnows in
the midwestern
and southwestern
United
States (Matthews, 1985). It is tolerant of harsh
environmental
conditions
(Matthews and Hill,
1979; Matthews, 1987), exhibits great vagility
(Deacon, 1961), and can invade or repopulate
marginal habitats rapidly (Cross and Collins,
606
vol.47, i). 4
'The Southwestern Naturalist
1995). It is considered a serious threat to native fish species in river systems outside its natural range (Minckley, 1973; Burr and Page,
1986; Greger and Deacon, 1988; Douglas et al.,
1994).
In species considered successful colonizers,
early age at maturity is an expected life history
attribute (Lewontin, 1965; Roff, 1992), and
rapid maturation under laboratory conditions
has been reported for C. lutrensis (Islam, 1972).
In nature, C. lutrensis matures between 24 and
30 mm standard length (SL) (Hubbs and Ortenburger, 1929; Cross, 1950; Farringer et al.,
1979), and Matthews (1988) suggested that individuals spawning in late summer in the Canadian River in Oklahoma might be young-ofyear, based on their size. Although Farringer et
al. (1979) showed that Oklahoma populations
of C. lutrensishad spawning peaks in early summer and again in August, and raised the possibility that some individuals might spawn during their first year, they concluded that age-0
spawning, if it occurred, was likely rare. Herein
we report production of larvae in large outdoor artificial streams in August by C. lutrensis
individuals hatched in April or May of the
same year.
Age-0 reproduction has also been suspected
in other cyprinids. Cowell and Barnett (1974)
reported that taillight shiner, Notropis maculatus, hatched in March or April in central Florida spawned in September at 6 mo of age, but
they based this conclusion on length-frequencies of a repeatedly sampled population and
had no information on age of individual fish.
Heins and Clemmer (1976:376) speculated
that "a small number of females" of longnose
shiner, Notropis longirostris,in Mississippi might
spawn in the first year of life but had no direct
evidence. Thus, age-0 reproduction had been
suspected or suggested for several North American cyprinid species, but never confirmed.
On 18 May 1999, at the end of an experiment on effects of C. lutrensis on stream productivity (Gido and Matthews, 2001), C. lutrensis larvae were collected with light traps (similar to those used by Floyd et al., 1984) from 10
of 14 outdoor artificial stream units that contained adult fish (captured October 1998 from
the Washita River, Carter County, Oklahoma).
Larvae were preserved and measured to the
nearest 0.1 mm SL under a dissection microscope. On 19 May 1999, all adults and juveniles
35
6 30
o
- 25
0
0.
* 0.
20
0
E
-
15
10
*0
.-
...
May
.I 1 I I I
Jun
I I
-
Jul
I
Aug
I. .t
Sep
- . . .. I I '
I
Oct
Nov
'I
Dec
Date (1999)
FIG. 1-Mid-day water temperatures in experimental unit 1 at the University of Oklahoma Biological
Station, MarshallCounty,Oklahoma.
(those large enough to be captured with a 3.2mm mesh seine) were removed from the 14
units. The only fish remaining were larvae or
extremely small juveniles (those that escaped
capture by light traps) hatched in the artificial
stream units in spring 1999. Removal of adults
and larger juveniles was confirmed by repeated
observations through plexiglass viewing ports
in each pool unit and by observation from
above in all shallows.
Spring-hatched C. lutrensisgrew undisturbed
in experimental units through summer 1999.
Fish were visually censused on 9 occasions between 19 May and 29 August, at intervals ranging from 4 days to 4 weeks. Counts and notes
on maximum size (SL) and breeding color of
individuals were made as conditions (e.g., visibility) permitted, but fish were not handled
until 29 August.
Conditions in experimental units closely approximated those in natural streams (Gido et
al., 1999; Gido and Matthews, 2001). Each experimental unit consisted of 1 pool, 183-cm diameter and 45 cm deep, and 1 narrow (45 cm)
shallows area, 122 cm long and ca. 15 cm deep
(figure in Gido and Matthews, 2001:248). Experimental units contained gravel and cobble
from a nearby stream. There was no flow or
aeration of water. Tanks were filled from the
local, treated, rural water supply on several occasions to maintain water levels. Midday water
temperature in Unit 1 was measured 14 times
from May through early November (Fig. 1).
From May though September, temperatures
(23.5 to 34.1?C) were similar to summer temperatures in streams occupied by C. lutrensisin
receIlmbe 200()2
607
Notes
350
c0
300 ?
->
110 .
-0
D 90C5
a)
('
130-
2 250(CO
4- 2000
,/
)
70 -
E
C 50 - -._
I_r
U) 30 -
Total number observed
Number of males with nuptial coloration
O
)
3
Z
?r-if H
10-
MayI
z
Jun
l
......!
Jul
-,
r7
Il
Aug
II
.. .
1r.
. .
Sep
.
.
150100 50-
0
*,
Date (1999)
of spring-hatched Cyprinella luFI(;. 2-Number
trensis captured (19 May and 29 August) or visually
estimated (all other dates) in experimental units
from 19 May to 29 August 1999 (closed circles).
Number of males with nuptial color observed 25
July, 2 August, and 10 August, or captured 29 August
(shaded bars).
I
I
.Q
'3
Co
'3
3
Oct
0
I
'3
I
~
o?
1
I
I'l
I
0I
5,
Co
Date (1999)
FIG. 3-Numbers of larvae (offspring of springhatched Cyprinellalutrensis) observed in experimental units from 29 August to 3 November 1999.
1999, when 118 individuals were captured and
redistributed among experimental units (Fig.
2).
Spring-hatched C. lutrensisgrew through the
Oklahoma (Matthews, 1977, 1987). The tem- summer. Larvae captured in light traps on 18
perature decline in Unit 1 from late SeptemMay 1999 ranged from 3.1 to 8.6 mm SL (x =
ber to early November mimicked that reported
5.1 ? 1.6 SD); larvae captured on 19 May by
by Matthews and Hill (1979) for C. lutrensis seine ranged from 6.9 to 8.8 mm SL (x = 8.0
habitats in Oklahoma. Food consisted of aquat- + 0.5 SD). Some spring-hatched individuals
ic invertebrates, attached algae, zooplankton,
left in experimental units were estimated to be
or winged adult insects available in experimen>30 mm SL by 6 July 1999. Those captured
tal units. Benthic core samples in May indicat- and measured on 29 August ranged in size
ed an abundance of aquatic invertebrates
from 22 to 39 mm SL (x = 30.6 + 3.4 SD).
A male with nuptial color was observed on
(Gido and Matthews, 2001). There was no sup25 July (Fig. 2). Additional males in breeding
plemental feeding.
On 29 August, we netted, measured (SL), color were observed on 2 August and 10 August. Of 118 spring-hatched individuals capfin-clipped, and released the spring-hatched
fish back into experimental units (n = 15), tured on 29 August, 26 were males with at least
where they remained until 15 October. We also some nuptial color, 8 of which had "high" colnoticed several newly-hatched individuals, 6 of or (Matthews, 1995).
On 29 August, we observed courtship in 2
which we captured with aquarium nets (ca. 1mm mesh) and measured from digital photoexperimental units, found recently-laid eggs on
stones in 2 units, and stripped mature to ripe
graphs. In subsequent weeks, visual censuses
were conducted to count larvae in all experi- eggs (Heins and Rabito, 1986) from 3 females
mental units. On 3 November 1999, all off- that ranged in size from 28 to 31 mm SL. On
spring of spring-hatched individuals were net- 29 August, we also found 6 recently-hatched C.
ted from experimental units, counted, and re- lutrensis (8.5 to 12.0 mm SL) in 3 units, offturned to experimental units.
spring of spring-hatched individuals.
On 18 and 19 May 1999, 88 larvae and small
Spring-hatched individuals continued to
were
and
10
from
juveniles
captured
preserved
produce offspring after 29 August (Fig. 3).
experimental units: 49 in light traps and 39 by Newly-hatched larvae were observed until 25
seine. Subsequent visual censuses consistently
October, 10 days after spring-hatched individestimated more than 110 spring-hatched indi- uals had been removed. On 3 November, 305
viduals in experimental units until 29 August offspring of spring-hatched individuals were
608
The SouthwesternNaturalist
recovered from all units. At that time, those
fish (hatched late summer to autumn) ranged
in size from approximately 8.5 to 31 mm SL.
Survival of these offspring in experimental
units was >90% from 3 November 1999 to 3
May 2000.
Estimated age of larvae captured 19 May
ranged from 0 to 28 days. Size at hatching for
C. lutrensis ranges from approximately 3.0 (Islam, 1972; reported as total length) to 4.5 mm
SL (Saksena, 1962). The smallest larva we captured on 18 May 1999 was 3.1 mm SL, suggesting this larva was newly hatched. We estimated age of the largest larva captured on 19
May (8.8 mm SL) to be 25 to 28 days based on
a study by Saksena (1962), who reported laboratory-hatched C. lutrensisreached 8.4 and 9.4
mm SL by Day 25 and Day 30, respectively. Because laboratory temperature in Saksena's
study (25 to 27.8?C) was higher than that observed in experimental units in May, and size
at hatching reported by Saksena (1962) was
larger than the size of our smallest captured
larvae, the largest larva captured on 19 May
might have been older than 28 days. A hatch
date in late April for the largest larva found on
19 May is consistent with the April onset of C.
lutrensis reproduction in Oklahoma streams
(Cross, 1950; Farringer et al., 1979).
There were likely unhatched eggs in the experimental units on 19 May 1999. If eggs were
laid immediately prior to removal of adults,
probable hatch date was 22 or 23 May, based
on mid-day temperatures in experimental units
of approximately 24?C and estimated hatching
time of 3.0 to 3.5 d (Islam, 1972).
Hubbs and Ortenburger (1929) reported
that C. lutrensis in natural populations mature
between 24 (the smallest mature female) and
30 mm SL. Several spring-hatched individuals
in experimental units were >30 mm SL by 6
July. If these individuals were also the oldest,
their growth rate in the artificial stream (assuming hatch date of 21 April and hatch size
of 3.1 mm SL) would have been approximately
0.34 mm/d, matching that reported by Islam
(1972) for laboratory-reared C. lutrensis. By 29
August, the mean size of spring-hatched individuals was >30 mm SL.
We observed courtship and spawning by
spring-hatched individuals in late August, but
the first evidence of maturity in these individuals was observation of a male in breeding col-
vol. 47, no. 4
or on 25 July. The size of the largest larva captured on 29 August (12.0 mm SL) also suggested that some spring-hatched individuals
were spawning by late July. Saksena (1962)
found that laboratory-reared larvae raised at
temperatures ranging from 25 to approximately 28?C (similar to mid-day artificial stream
temperatures in late July) reached 9.4 and 15.0
mm SL by Days 30 and 34, respectively. Thus,
the largest larva captured on 29 August might
have hatched as early as 29 July.
Reproduction by spring-hatched individuals
continued until they were removed from experimental units in mid-October, and might
have continued later into autumn (based on
observed reproductive condition at the time of
removal). Spawning season for C. lutrensis, as
reported in the literature, typically ends in late
summer (Carlander, 1969; Cavin, 1971; Farringer et al., 1979), although Cross (1967) noted
that spawning continued into October in Kansas. Later autumnal reproduction in natural
populations was suggested by Matthews (1988)
and Fausch and Bestgen (1997), who found individuals as small as 14 to 15 mm in the field
in late winter and early spring. Matthews
(1988) also suggested that individuals spawning in late summer and autumn might be
young-of-year.
Spawning by young-of-year C. lutrensismight
substantially influence natural population
growth if larvae produced in late summer or
autumn survive the winter. Survival of late summer/autumn-hatched larvae retained over winter in our experimental units was extremely
high. These fish were not exposed to predation
by other fish species, however, and overwinter
survival in nature is likely lower than we observed. There is also circumstantial evidence
that young produced in late summer or autumn overwinter successfully in the wild; in
February 2000, the mean size of 894 red shiners captured from a single school in the Washita River, Kiowa County, Oklahoma, was 18.3
mm SL (Matthews et al., 2001).
Our observation of spawning and successful
reproduction by C. lutrensisin the first summer
of life provides insight into success of introduced populations of this species in much of
the Colorado River system of the American
Southwest, where it is suspected to impact native fishes though competitive displacement
(Douglas et al., 1994) and predation (Ruppert
December 2002
Notes
et al., 1993; Gido et al., 1999; but see Brandenburg and Gido, 1999). The ability of C. lutrensis
to occupy a variety of habitats (Matthews and
Hill, 1980; Cross and Collins, 1995), including
those with harsh conditions, has presumably
enabled this species to persist where it has
been introduced and even to occupy modified
habitats unsuitable for native species (Deacon
et al., 1987). Early reproduction and short generation time might allow production of 2 generations per year (in some, if not all, years).
This, coupled with the production of multiple
clutches within a breeding season (Gale,
1986), might explain why introduced C. lutrensis have become numerically dominant at many
sites where they have become established
(Hubbs, 1954; Gido et al., 1997).
Resumen-El 19 de mayo de 1999 se encontraron juveniles de Cyprinellalutrensisde aproximadamente 9 mm de longitud total, en unos
tanques experimentales al aire libre en la Estaci6n Biol6gica de la Universidad de Oklahoma.
Se estima que los j6venes nacieron a fines de
abril o principios de mayo, de peces adultos utilizados en un experimento durante el invierno
anterior. El 19 de mayo todos los peces adultos
se removieron de los tanques pero los j6venes
eran demasiado pequeiios para ser capturados
y removidos, por lo que permanecieron ahi durante todo el verano. En agosto de 1999, varios
de estos j6venes habian alcanzado el tamafno y
la coloraci6n de los machos reproductivos. El
29 de agosto del mismo afio se observaron huevos y crias recien nacidas en los tanques. Estas
observaciones demuestran que las crias de Cyprinella lutrensisnacidas en mayo son capaces de
reproducirse en el primer verano de su vida, a
una edad aproximada de 120 dias. La maduraci6n rapida y el tiempo generacional corto pueden contribuir a la habilidad de esta especie
para establecerse rapidamente en los sitios a
donde se introducen.
We thank A. T. Marshfor assistancein setting up
the initial experiment, D. Cobb for assistancemaintaining the experiments, and D. C. Heins for discussions of reproduction in minnows. M. Lourdes Romero-Almeraztranslated the resumen. The research
on fish effects in ecosystemsfrom which this report
is derived was approved by the Institutional Animal
Care and Use Committee, University of Oklahoma;
field sampling was under permit by Oklahoma Department of Wildlife Conservation.
609
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Submitted8 May 2001. Accepted31 December2001.
AssociateEditor was David L. Propst.