Content uploaded by Jeremy S. Tiemann
Author content
All content in this area was uploaded by Jeremy S. Tiemann on Aug 19, 2014
Content may be subject to copyright.
SPAWNING BEHAVIOR OF THE SLIM MINNOW, PIMEPHALES TENELLUS
JEREMY S. TIEMANN
Illinois Natural History Survey, Division of Biodiversity and Ecological Entomology, Champaign, IL 61820
Correspondent: jtiemann@inhs.uiuc.edu
ABSTRACT—Little is known about the life history and habits, including the reproductive behavior, of
Pimephales tenellus. I collected 182 individuals and transferred them into 10 aquaria; of these fish, 18
pairs spawned. Based on my aquarium observations, P. tenellus exhibited the egg-clustering strategy
similar to the other species of Pimephales.
RESUMEN—Existe informacio´n limitada sobre la historia de vida y los ha´ bitos de Pimephales tenellus,
incluyendo su comportamiento reproductivo. Colecte´ 182 individuos y los transferı´ a 10 acuarios; de
estos peces, 18 pares desovaron. Basa´ndome en mis observaciones de los peces en acuarios, P. tenellus
exhibe una estrategia de agrupacio´n de huevos que es similar a la de las otras especies de Pimephales.
The slim minnow, Pimephales tenellus, occurs in
schools in the midwater or near the streambed of
mid-sized streams that have clean sand-gravel-
cobble bottoms and moderate flowing water in
the Red and Arkansas river drainages and other
tributaries of the Mississippi River in the Ozarks
and adjacent regions of Arkansas, northeastern
Oklahoma, southern Missouri, and eastern Kan-
sas (Page and Burr, 1991). Little is known about
the habits and life history (e.g., spawning behav-
iors) of P. tenellus.Pimephales are broadly sympat-
ric and normally syntopic, but often separate by
slight habitat differences (Cross, 1967), and based
on aquarium observations, Pimephales have
evolved reproductively associated morphological
features and complex breeding behaviors (e.g.,
egg-clustering breeding strategy) (Page and Ceas,
1989). Unlike the other Pimephales species, P.
tenellus often actively swim in the current, and
therefore could occupy different breeding habi-
tats than observed for the other 3 Pimephales
species: bluntnose minnow, P. notatus; fathead
minnow, P. promelas; and bullhead minnow, P.
vigilax. Cross (1967) suggested that P. tenellus
spawns among rocks in fast water from May to
July, when water temperatures range from 24 to
29uC, and Page and Ceas (1989) proposed that P.
tenellus employs an egg-clustering breeding strat-
March 2007 Notes 137
egy similar to that of the other Pimephales species.
However, P. tenellus reproduction has not been
documented. The objective of this study was to
describe P. tenellus spawning behavior.
I collected 31 age-0 P. tenellus on 22 December
2003 and 151 age-0 and older P. tenellus on 25
February 2005 in the Neosho River in Emporia,
Lyon County, Kansas. I vouchered one fish in the
Illinois Natural History Survey Fish Collection,
Champaign (INHS 97877). I divided the remain-
ing fish into 10 aquaria (six 40 L, one 60 L, one
130 L, one 150 L, and one 210 L) that were
housed in a room with little human traffic.
Because age-1 Pimephales successfully have
spawned in ponds (Markus, 1934), the 40-L
aquaria contained only age-1 and older fish
collected in 2005, whereas the other aquaria had
a combination of age-0 and older fish (stocking
densities below).
I placed most substrates known for North
American minnows in each aquarium (Page and
Johnston, 1990), including sand; gravel; pebble;
cobble arranged to create narrow crevices (to
3 cm); logs with crevices and exposed under-
surfaces; paired valves of 5 freshwater mussel
species (Amblema plicata,Fusconaia flava,Lasmi-
gona complanata,Potamilus alatus, and Quadrula
quadrula) known to occur in the range of the
fish; and various sizes of 3 taxa of aquatic plants
(Ceratophyllum,Najas, and Potamogeton). I kept
proportions of substrates and densities of fresh-
water mussels similar to that found at the point
of collection (see Dean et al., 2002; Tiemann et
al., 2004).
I kept aquaria at ambient light and tempera-
ture conditions, except I did not allow water
temperature to fall below 10uC. Photoperiod
varied from 10L:14D to 16L:8D, and water
temperature varied from 10 to 26uC during the
study. I provided some flow, approximately
0.25 m/s measured with a Swoffer Model 2100
current meter (Swoffer Instruments, Inc., Seat-
tle, Washington), at the surface of the substrate
by using Fluval 3+underwater filters (Rolf C.
Hagen Corp., Mansfield, Massachusetts).
Low population densities (0.09 to 0.26 fish/L
in aquaria) and high feeding rates increase
Pimephales growth, gamete development, and
egg size (Smith et al., 1978). Therefore, I stocked
fish at approximately 0.20 fish/L in the 60-L,
130-L, 150-L, and 210-L aquaria; 3 of the 40-L
aquaria each had one male and one female, and
3 of the 40-L aquaria each had one male and 3
females. I fed fish (ad lib.) a combination of
Hikari brine shrimp, Hikari micro-pellets, and
Hikari crushed algae wafers (Hikari Sales, Inc.,
Hayward, California) 5 d/wk and frozen chiron-
omid larvae 1 d/wk (I fasted fish 1 d/wk). I
observed fish on a daily basis 30 min in the
morning around sunrise and 30 min in the
evening at sunset. Because Pimephales spawn at
night (Gale, 1983), I videotaped the 130-L
aquarium 24 h/d throughout the spawning
season. I also observed fish for 15 min every
3 h twice a week during the spawning season. I
turned on a red light prior to the dark cycle to
allow nighttime behavioral observations (see
Bulger et al., 2002).
All Aquaria—The timing of peak gonad weight
was not measured; however, gonosomatic index
scores for Pimephales are low throughout winter
and increase with changing physicochemical
parameters as the spawning season nears (Smith,
1977). Age-1 and older P. tenellus started showing
signs of sexual maturity around the middle of
April, as photoperiod neared 15L:9D and water
temperature approached 16uC. Females devel-
oped an enlarged urogenital structure and
continued schooling behavior, but males, who
were larger than females, shifted from schooling
behavior to territoriality. Males developed sec-
ondary sexual characteristics, including a swollen
black head, breeding tubercles on snout, a thick-
ened first dorsal ray, and dorsal pad on nape and
spine. The dorsal pad in a Pimephales male
contains goblet cells that secrete mucus to
chemically mark the nest and taste buds that
allow chemosensory sampling of the nest (Smith
and Murphy, 1974). Induced by peak androgen
production, the dorsal pad contains no alarm
substance cells to prevent possible discharge of
shreckstoff during nesting (Smith, 1973), but
individuals retain the advantage of detecting and
responding to shreckstoff if it is emitted from
another fish (Smith, 1976).
After developing the secondary sexual char-
acteristics, P. tenellus males established a nest
within a crevice of submerged cobble. Larger
males tended to have larger nests. When estab-
lishing a nest, males used various visual and
contact displays (hovering, circling, rubbing, and
nibbling) and seldom (mean ,1/30 min of
viewing) left their nest. Males then courted
females by using various visual and contact
displays (approaching, lateral displaying, tap-
ping, and leading). Pimephales can produce
138 The Southwestern Naturalist vol. 52, no. 1
sound and release water-borne chemicals during
spawning (Cole and Smith, 1987; Cole and
Smith, 1992; Johnston and Johnson, 2000).
One pair of age-1 P. tenellus spawned on 14
May 2004 and at least 17 pairs of age-1 and older
spawned between 15 and 21 May 2005. The onset
of spawning for both years occurred at approx-
imately 16L:8D photoperiod and 24uC water
temperature; all spawning took place shortly
(about 15 min) before sunrise. Mean (6SD)
spawning time was 7 62 min and mean (6SD)
spawning season was 7 60d.
Some post-spawning mortality of age-1 and
older P. tenellus occurred for males but not
females. In Pimephales, reduced feeding during
the spawning season, combined with excess energy
expenditure while undergoing physiological
changes associated with development of second-
ary sex characteristics and excess energy expen-
diture while fighting intruders during nesting,
decreases immunity and results in increased post-
spawning mortality (Gale and Buynak, 1982).
130-L Aquarium Video Observations—When
ready to spawn, a P. tenellus female entered and
examined the nest of a male. She then turned on
her side and allowed the male to juxtapose
himself below her. The pair remained pressed
together on their sides and simultaneously swam
in circles while undulating. It was during this
process that the female pressed adhesive eggs,
which simultaneously were fertilized by the male,
one-by-one in a single-layer cluster on the un-
derside of cobble. To do so, the female released
an egg from her genital papilla, rolled it along the
upper side of her body, and pressed it to the
underside of the submerged object while she was
on her side and the male was pushing against her.
After spawning, the P. tenellus female left and
the male spent the majority of his time within
5 cm of the nest and did not leave his nest to
court new females; the only time he left was
during feedings. The male vigorously defended
his nest against intruders (usually other males)
by using various visual and contact displays
(biting, head-butting, chasing, tail-beating, car-
ouselling, charging, and fin erection); however,
the male did not assume a banding pattern on
the body as seen in other Pimephales species (e.g.,
McMillian and Smith, 1974). The single-layer
clustering of eggs allows the male to easily care
for them (Page and Ceas, 1989). To do so, the P.
tenellus male rubbed his dorsal pad and thick-
ened first dorsal ray over the eggs about once per
every 30 min of viewing. These acts spread, turn,
clean, and aerate the eggs (Page and Ceas,
1989). During this contact, goblet cells in the
dorsal pad of the Pimephales male secrete mucus
onto the nest that serves as protection for the
eggs against abrasion and disease (Smith and
Murphy, 1974). In the nest, the P. tenellus male
removed dead eggs (opaque in color) from the
clutch. Visual stimuli aid in removal of dead eggs
in Pimephales nests (McMillian and Smith, 1974).
Three 40-L Aquaria—The one male-one female
aquaria allowed observations on P. tenellus female
breeding. After each observed spawning, the roof
of the nest was removed, the number of eggs were
counted, a subsample of eggs (n5200 total) was
taken to determine size and development rates,
and the roof was replaced; the male returned to the
nest after the roof was replaced. The subsampled
eggs were arranged in a wire basket, soaked for
5 min in a betadine solution to disinfect the surface
oftheeggs,andplacedintoaseparate40-L
aquarium for observations of development. All 3
females exhibited fractional spawning; 2 of the
females laid 2 clutches of eggs, whereas the third
female laid 3 clutches. Larger females deposited
more eggs, as was observed in other aquaria. For all
3 females, 2 d elapsed between the first and second
spawning sessions; 5 d elapsed between the second
and third spawning sessions for the one female.
The mean (6SD) first clutch size was 189 621
eggs, whereas the second was 151 617 eggs; the
third clutch size for the one female was 89 eggs.
Often Pimephales nests have eggs that are in various
stages of development (Wynne-Edwards, 1932).
Fractional spawning not only allows the female to
increase her fecundity by producing more eggs in
a season than possibly could be held, but also
decreases the chance that an entire generation will
be eliminated by short-term environmental events
(Gale and Buynak, 1982).
Three 40-L Aquaria—The one male-3 female
aquaria allowed for observations of P. tenellus male
breeding, as well as female egg laying behavior.
The females in each aquarium were distinctively
marked with a unique color code using tetracy-
cline. All 3 males exhibited polygamy and bred
asynchronously. Two of the males spawned with 2
females, whereas the third male spawned with all
3 females. All 3 males continuously spawned while
caring for their eggs (e.g., removing diseased eggs
from their clutch). The number of eggs in a nest
seemed to be limited by nest size, which is
common in Pimephales (Sargent, 1989).
March 2007 Notes 139
Allopaternal care evolved in Pimephales (Unger
and Sargent, 1988). However, P. tenellus males
were not given a choice to adopt nests, so it was
unknown whether nest adoption and allopater-
nal care is part of the reproductive strategy of the
male, and whether allopaternal care and egg
survival increase with increasing clutch size. Both
of the above have been documented in Pime-
phales (Sargent, 1988; Unger and Sargent, 1988).
Although a male exhibiting allopaternal care
often pays an extra energy cost in caring for
adopted eggs, having the ability to discriminate
(e.g., giving less care, defending less vigorously,
and exploiting as a food source) between sired
and adopted eggs could be beneficial to attract
females and sire his own offspring (Sargent,
1989). In all aquaria, it was unknown whether P.
tenellus females preferred males with eggs in their
nests, as is common in Pimephales. The presence
of eggs in a nest is an indication that the
guarding male provides successful care (Unger
and Sargent, 1988; Sargent, 1989).
Egg Development—The subsampled P. tenellus
eggs were spherical, transparent, and 1.20 mm
(60.05 mm SD) in diameter. Incubation period
was about 6 d (61dSD)at24uC. Twenty-four of
the subsampled eggs hatched. Fry were milky-
white in color and were 4.65 mm (60.10 mm
SD) mm in length. Fry emerged from the eggs
both headfirst and tail-first, and vigorously
wiggled to separate from the egg. When freed,
fry drifted to the bottom and remained motion-
less for 1.5 d (presumably until their air bladders
filled). For the next 3.5 d, fry emerged from the
substrate only at night. Fry then began schooling
7 d after hatching. Fry apparently receive no
paternal care and are often eaten by their
parents (McMillian and Smith, 1974).
Based on my aquarium observations, P. tenellus
exhibited the egg-clustering breeding strategy
similar to the other Pimephales species (Page and
Ceas, 1989). However, my observations were in
an artificial setting, which could differ from what
occurs in the wild. Growth and fecundity in
Pimephales are influenced by population density,
food supply, habitat, physicochemistry, and in-
festation of parasites (Smith et al., 1978). In
nature, these factors might have caused differ-
ences in life history attributes.
L. M. Page (Florida Museum of Natural History)
provided the idea for this project. Partial funding for
this project came from the Illinois Department of
Transportation. The Kansas Department of Wildlife
and Parks issued a collecting permit. S. D. Baker and D.
R. Edds (Emporia State University) assisted in collect-
ing. B. L. Tiemann assisted in fish care. B. Molano-Flores
(Illinois Natural History Survey) edited the resumen. S.
D. Baker, D. R. Edds, and B. L. Tiemann; K. R. Bestgen
and S. A. Flickinger (Colorado State University); G. A.
Levin, C. A. Phillips, M. E. Retzer, and D. L. Thomas
(Illinois Natural History Survey); and 3 anonymous
reviewers provided constructive criticism.
LITERATURE CITED
BULGER, A. G., M. WILDHABER,AND D. EDDS. 2002. Effects
of photoperiod on behavior and courtship of the
Neosho madtom (Noturus placidus). Journal of
Freshwater Ecology 17:141–150.
COLE, K. S., AND R. J. F. SMITH. 1987. Release of
chemicals by prostaglandin-treated female fathead
minnows, Pimephales promelas, that stimulate male
courtship. Hormones and Behavior 21:440–456.
COLE, K. S., AND R. J. F. SMITH. 1992. Attraction of female
fathead minnows, Pimephales promelas, to chemical
stimuli from breeding males. Journal of Chemical
Ecology 18:1269–1284.
CROSS, F. B. 1967. Handbook of fishes of Kansas.
University of Kansas Museum of Natural History
Miscellaneous Publication Number 45, Lawrence.
DEAN,J.,D.EDDS,D.GILLETTE,J.HOWARD,S.SHERRADEN,
AND J. TIEMANN. 2002. Effects of lowhead dams on fresh-
water mussels in the Neosho River, Kansas. Transac-
tions of the Kansas Academy of Science 105:232–240.
GALE, W. F. 1983. Fecundity and spawning frequency of
caged bluntnose minnows – fractional spawners.
Transactions of the American Fisheries Society
112:398–402.
GALE, W. F., AND G. L. BUYNAK. 1982. Fecundity and
spawning frequency of the fathead minnow –
a fractional spawner. Transactions of the American
Fisheries Society 111:35–40.
JOHNSTON, C. E., AND D. L. JOHNSON. 2000. Sound
production in Pimephales notatus (Rafinesque) (Cy-
prinidae). Copeia 2000:567–571.
MARKUS, H. C. 1934. Life history of the blackhead
minnow (Pimephales promelas). Copeia 1934:116–122.
MCMILLIAN, V. E., AND R. J. F. SMITH. 1974. Agonistic and
reproductive behaviour of the fathead minnow
(Pimephales promelas Rafinesque). Zeitschrift fur
Tierpsychologie 34:25–58.
PAGE, L. M., AND B. M. BURR. 1991. A field guide to
freshwater fishes of North America north of
Mexico. Houghton Mifflin, Boston, Massachusetts.
PAGE, L. M., AND P. A. CEAS. 1989. Egg attachment in
Pimephales (Pisces: Cyprinidae). Copeia 1989:1074–
1077.
PAGE, L. M., AND C. E. JOHNSTON. 1990. The breeding
behavior of Opsopoeodus emiliae (Cyprinidae) and its
phylogenetic implications. Copeia 1990:1176–1180.
140 The Southwestern Naturalist vol. 52, no. 1
SARGENT, R. C. 1988. Paternal care and egg survival both
increase with clutch size in the fathead minnow,
Pimephales promelas. Behavioral Ecology and Socio-
biology 23:33–37.
SARGENT, R. C. 1989. Allopaternal care in the fathead
minnow, Pimephales promelas: stepfathers discrimi-
nate against their adopted eggs. Behavioral Ecology
and Sociobiology 25:379–385.
SMITH, H. T., C. B. SCHRECK,AND O. E. MAUGHAN. 1978.
Effect of population density and feeding rate on the
fathead minnow (Pimephales promelas). Journal of
Fish Biology 12:449–455.
SMITH, R. J. F. 1973. Testosterone eliminates alarm
substance in male fathead minnows. Canadian
Journal of Zoology 51:875–876.
SMITH, R. J. F. 1976. Male fathead minnows (Pimephales
promelas Rafinesque) retain their fright reaction to
alarm substance during the breeding season.
Canadian Journal of Zoology 54:2230–2231.
SMITH, R. J. F. 1977. Seasonal changes in the histology
of the gonads and dorsal skin of the fathead
minnow, Pimephales promelas. Canadian Journal of
Zoology 56:2103–2109.
SMITH,R.J.F.,AND B. D. MURPHY. 1974. Functional
morphology of the dorsal pad in fathead minnows
(Pimephales promelas Rafinesque). Transactions of
the American Fisheries Society 103:65–72.
TIEMANN, J. S., D. P. GILLETTE,M.L.WILDHABER,AND D. R.
EDDS. 2004. Effects of lowhead dams on riffle-
dwelling fishes and macroinvertebrates in a Midwest-
ern river. Transactions of the American Fisheries
Society 133:705–717.
UNGER, L. M., AND R. C. SARGENT. 1988. Allopaternal care
in the fathead minnow, Pimephales promelas: females
prefer males with eggs. Behavioral Ecology and
Sociobiology 23:27–32.
WYNNE-EDWARDS,V.C.1932.Thebreedinghabitsofthe
black-headed minnow (Pimephales promelas Raf.). Trans-
actions of the American Fisheries Society 62:382–383.
Submitted 27 August 2005. Accepted 20 April 2006.
Associate Editor was Gary Garrett.
March 2007 Notes 141