Morphology and development of the postcranial skeleton in the channel catfish Ictalurus punctatus (Ostariophysi: Siluriformes)

40 Pages·2 MB·English

by  Grande, Terry

590.5
Biology
FI
N.S.
99
Jun 28, 2002
OpiTJv
the hannel Cattish
l
ophysi: Siluriformes)
ieldiana
2 (Permanence of Paper).
FIELDIANA
Zoology
NEW
SERIES, NO. 99
Morphology and Development of the
Postcranial Skeleton in the Channel Catfish
Ictalurus punctatus (Ostariophysi: Siluriformes)
Terry Grande Judith D. Shardo
Associate Professor DepartmentofBiological Sciences
Department ofBiology University ofSouth Alabama
Loyola University 124 Life Sciences Building
6525 North Sheridan Road Mobile, Alabama 36688
Chicago, Illinois 60626 U.S.A.
U.S.A.*
ResearchAssociate
Department ofGeology
FieldMuseum ofNatural History
1400 South Lake Shore Drive
Chicago, Illinois 60605-2496
U.S.A.
*Addressforcorrespondence.
WS/0L0GY
LIBRARY
Accepted January 16, 2002 Bimu HAH
Published June 28, 2002
Publication 1518 NOV 1 9 2002
PUBLISHED BY FIELD MUSEUM OF NATURAL HISTORY
2002 Field Museum of Natural History
ISSN 0015-0754
PRINTED IN THE UNITED STATES OF AMERICA
Table of Contents 2. Early formation of vertebral proto-
centra 9
3. Development of the caudal fin
Abstract
1 skeleton 9
Introduction 2
4. Development of the anal fin skeleton .... 13
Methods 2
5. Development of the median fins and
Skeletal Preparation 2 axial skeleton 16
HDiesvteolloopgimceanltaalndStSaEgiMngPrMeeptahroatdion 33 6. Development of the vertebral column .... 17
Materials 3 7. Formation ofcaudal fin epurals and
Developmental Series Examined 3 neural spines 19
Adult Materials Examined 4 8. Intraspecific variation in caudal fin
Abbreviations 4 structure 20
Results 4 9. Development of the Weberian appara-
Developmental Staging 5 tus/dorsal fin unit 22
Discussion 14 10. Development of the dorsal fin spines .... 23
Overview of Median Fin Fold Formation 1 1. Adult anterior vertebral region, lateral
and Development 14 view 25
Overview of Paired Fin Development 15 12. Adult anterior vertebral region, dorsal
Development of the Caudal Fin and ventral views 26
Skeleton 18
Development of the Weberian Apparatus/
Dorsal Fin Unit 21
Variation in Development 27
Acknowledgments 28 List of Tables
Literature Cited 28
List of Illustrations 1. Summary of specimen sampling corre-
lated with the first occurrence of defin-
ing criteria 5
1. Scanning electron micrograph of the 2. List of defining and concurrent charac-
development of Ictaluruspunctatus ters for stages 1-18 6
111

Morphology and Development of the Postcranial
Skeleton in the Channel Catfish Ictalurus punctatus
(Ostariophysi: Siluriformes)
Terry Grande1 Judith D. Shardo2
Abstract
The morphology and development ofthe postcranial skeleton ofthree independent series
of the channel catfish Ictalurus punctatus were studied using a combination of techniques
(histology, SEM, skeletal clearing and staining). More than 2,000 specimens ranging in
developmental stage from a fertilized egg to individuals about 400 mm TL were examined.
Our results show individual variation in the onset of the hatching and foraging periods,
and in the appearance or number of several skeletal structures (e.g., number of hypurals).
Our results also show that regardless of this variation, the sequence of development ofthe
postcranial structures is consistent within the series studied, and that the development of
these structures is correlated more with the size of the fish than with age. Because of the
consistent pattern of postcranial skeletal development observed, we were able to construct
an ontogenetic staging scheme consisting of 18 developmental stages, each characterized
by one defining criterion. Additional and more variable characters that occur concurrently
with each of the 18 defining criteria are identified as concurrent features. This staging
method facilitates future comparisons with the developmental patterns of other fish taxa,
and is independent of age.
As part ofthis study, careful developmental descriptions ofthe Weberian apparatus, vertebral
column, and paired and median fins were made. A primary goal of the study was to better
understand the developmental relationship between the Weberian apparatus and the dorsal fin
skeleton. Together they form an extremely unusual anatomical complex whose development
and function are tightly linked. During development, the fourth neural spine of the Weberian
apparatus forms a tight articulation with the first two proximal radials of the dorsal fin. In
catfishes that exhibit a similar modification of the dorsal fin, sound production has been im-
plicated.
Through detailed anatomical descriptions, this study examined contested homologies of the
vertebral column and caudal fin. Such homologies include the caudal fin epurals, which in
Ictaluruspunctatus form as independentelements that laterfuse tothe neural spines ofposterior
vertebrae. New terminology is suggested for several skeletal structures to reflect their devel-
opmental origin.
1 Associate Professor, Department of Biology, Loyola University, 6525 North Sheridan Road, Chicago, Illinois
60626; Research Associate, DepartmentofGeology,Field MuseumofNatural History, RooseveltRoadatLake Shore
Drive, Chicago, Illinois 60605-2496.
2Department ofBiological Sciences, University ofSouth Alabama, 124 Life Sciences Building, Mobile, Alabama
36688.
FIELDIANA: ZOOLOGY, N.S., NO. 99, JUNE 28, 2002, PP. 1-30 1
Introduction skeleton of /. punctatus exhibits considerable
morphological variation within and between the
Until recently, researchers examining patterns of developmental series examined. Despite this
vertebrate development, and more specifically actin- variation, consistent features of axial skeleton
opterygian development, focused on a handful of formation can also be identified, and the de-
"model species" (e.g., the zebrafish Danio rerio) to tailed developmental timing of particular skel-
make generalizations about the formation of mor- etal elements appears to correlate more closely
phological structures such as the neural tube and with the size of the fish than with its age.
vertebral column (Kuwada et al., 1990; Kimmel et Hypotheses about the evolution, development,
al., 1995). However, studies such as those ofSchul- function, and homologies ofdifferent elements of
tze and Arratia (1988, 1989), Bemis and Grande the Weberian apparatus have been proposed by
(1992), Arratia and Schultze (1992), Shardo (1995), many authors (e.g., Krumholz, 1943; Martin,
and Grande and Bemis (1998) have illustrated sig- 1963; Alexander, 1964; Rosen & Greenwood,
nificant variation in skeletal developmentwithin Ac- 1970; Gayet, 1986; Chardon & Vandewalle,
tinopterygii. Obviously, no one fish species can be 1997). Some of these hypotheses are in conflict
used as a model for all of Actinopterygii. with each other. For example, Coburn and Futey
This study describes the development of the (1996) argue that the claustrum in otophysans is
postcranial skeleton (post early cleavage stages) derived from the first supraneural, while Fink and
ofIctaluruspunctatus, commonly known as the Fink (1981) argue that the claustrum forms from
channel catfish, one of the most common ictal- a disassociated part of the first neural arch. As
urids in North America. Phylogenetically, /. part of our study we investigated various hypoth-
punctatus is considered by many researchers eses of Weberian apparatus formation in light of
(e.g., Lundberg & Baskin, 1969; Arratia, 1992; the new morphological data we obtained. Our ob-
de Pinna, 1996; Coburn & Grubach, 1998) to be servations show that the development of the We-
a relatively basal siluriform because it exhibits berian apparatus in /. punctatus is functionally
a primitive caudal fin and a relatively primitive linked to the development of the dorsal fin skel-
Weberian apparatus in comparison to other cat- eton. We term this functional unit the Weberian
fishes. On the other hand, as a siluriform, /. apparatus/dorsal fin unit, and explore some impli-
punctatus exhibits many modifications and bone cations of this unit as a stabilizer for the dorsal
fusions not present in outgroup ostariophysans fin spine. We also comment on its possible role in
such as cypriniforms, characiforms, and gon- sound transmission.
&
orhynchiforms (Rosen Greenwood, 1970;
Fink & Fink, 1981, 1996; Grande & Poyato-
Ariza, 1999).
Although specimens of adult catfishes are Methods
common in North American museum collec-
tions, developmental material and consequen- Skeletal Preparation
tially developmental studies are rare (e.g.,
Armstrong, 1962; Arratia, 1990, 1992; Kobay- Specimens were preserved in either 10% buff-
akawa, 1992; Adriaens, 1998; Coburn & Gru- ered formalin or 4% buffered paraformaldehyde.
bach, 1998). Studies of the development of /. Skeletal material was prepared using a modified
punctatus are rarer still, and have focused only version of Dingerkus and Uhler's (1977) tech-
on specific parts of the skeleton. For example, nique for staining and counterstaining bone and
Kindred (1919) and Eaton (1937) examined cartilage. In this method, bone is stainedwith aliz-
skull development, while Al-Rawi (1966) ex- arin red and cartilage is stained with alcian blue.
amined the early development of the Weberian Trypsin was used to render the soft tissue trans-
apparatus. The current study examined the de- parent. An ethyl alcohol series was substituted for
velopment of the entire postcranial skeleton the KOH step in the standard Dingerkus and
(vertebral column, Weberian apparatus, dorsal Uhler method because the larval specimens are
and caudal fins, and pectoral and pelvic fins) fragile. Once cleared and stained, the specimens
using three independent developmental series, were stored in glycerin. Specimens were dissect-
each from a single spawn, for a total of more ed, examined, and drawn under a Wild MZ8 dis-
than 2,000 specimens. We found that, contrary secting microscope. Total lengths (TL) were taken
to Lundberg and Baskin (1969), the caudal fin from all specimens. Standard lengths (SL) were
FIELDIANA: ZOOLOGY
recorded for specimens with defined caudal fin characters that occur concurrently with the defin-
supports. ing criterion ofa particular stage but are not nec-
essarily linked to the defining character are de-
fined as concurrent features (Shardo, 1995). This
Histological and SEM Preparation method ofdevelopmental staging allows forcom-
parisons with other species, regardless of the
5 mFomrmtaoli2n0-fmimxedTLspweecriemepnrsepraarnegdinfgorihnisstiozleogfircoaml length or age of the individuals being compared.
examination using one of two methods. To help
establish the onset of vertebral column ossifica-
tion, specimens were decalcified in De-cal (Na-
Materials
tional Laboratories), dehydrated in an ethyl alco-
hol series, cleared in xylene, embedded in paraf-
fin, and cut in 10-u,m-thick transverse or sagittal Developmental Series Examined
sections. To examine the morphology of the We-
berian apparatus and vertebral column, specimens Three independent developmental series of
were prepared using the low-viscosity nitrocellu- channel catfish were examined. Two separate se-
lose (LVN) embedding technique of Thomas ries were spawned from eggs obtained from
(1983). Specimens were decalcified in formic Osage Catfisheries (Osage Beach, Mo.). The third
acid, dehydrated in an alcohol series, and embed- series was spawned from eggs obtained from the
ded in a graded concentration series of LVN. Catfish Genetics Research Unit (U.S. Department
TarnaAnsmveerrisceanseOcpttiiocnasl48060u,smlidtihnigckmiwcerroetocmuet.uBsoitnhg oStfonAegvriillceu,ltMuirses,.).AgEraiccuhltduerveeloRpemseenatraclh seSreirevsicweass,
twmhiaittnhoxaaynlmdiondtihafincidkedphiivcsetrroosl-iopognoincocafleaHsuuemcptariosoconensd'uwsreer(.1e97s2t)aihnee-d rfmaaacitiseleildtyieatstheaatsdaaibmfofeuetrceon2nt6diClt)oi.coantSsieo(rnii.eeb.s,utAsiumwnuadlesarterdaaipsspetrdroexbaiym-
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catheodrieomnbwraysosreamnodvyeodlkassatchelafrirvsatestweepr.eDewcahsohreidoni-n rtahieseOdsabgyeBCeamtifsishlafbaocrialtitoyryanpdersoobntnaeilnewdorfkrionmgWa.t
sasqpouedecioiuummsecnascwoolaudstyiltoahnteenofbduef2hf%yedrroaasntmeddituthmehnrotpeuotgsrhtoxfaiindxeea.dlciEonahcaohln ECS.aetrBfiieessmhiCsFacw(iUalnsiitvyre.arisAsietdtyotboayflMoSafhsas2ra,dc2ho9u3satestpttehsce,imSAtemonhnseervs(it9l8)l5.e
series, treated with Peldri II, dried in air, coated specimens in series A, 258 specimens in series B,
with 400 A of gold/palladium (Young et al., 1,050 specimens in series C) were collected from
1995), and examined in a Cambridge 240 SEM. these series, ranging from newly fertilized eggs to
foraging subadults with ossified axial skeletons.
Samples of at least seven specimens were col-
Developmental Staging Method lected for 18 days (series B) and 30 days (series
A and C). At least four samples were preserved
Early ontogeny consists of growth and a se- each day within the collecting period. The number
quence of developmental changes over time. of samples and the frequency of collecting de-
These rates of growth and developmental change creased in all three series toward the last days of
are not necessarily constant or correlated with collecting, after mthme fish had achieved a total
each other. Thus, age or length does not consis- length of 35-40 or were foraging freely.
tently correspond to a level of development, par- All fish from series A are deposited in the fish
ticularly among different species (Fowler, 1970; collection at Loyola University, Chicago (LU
Reimchen & Nelson, 1987). For purposes ofcom- D081090). Illustrated specimens were assigned
parison, in this study the developmental sequence Loyola University (LU) catalogue numbers. Se-
ofthe axial skeleton is divided into morphological ries B is deposited in the University of Massa-
stages. Each stage is characterized by one mor- chusetts Ichthyological Collection, Amherst
phological feature that acts as the defining crite- (UAM Fl 1257), and seriesC is housed at the Uni-
rion (Shardo, 1995). Additional and more variable versity ofSouth Alabama, Mobile (USA 040645).
GRANDE & SHARDO: POSTCRANIAL SKELETON IN ICTALURUS PUNCTATUS
Adult Materials Examined
Materials examined to assess the morphological
condition of the postcranial skeleton in larger
specimens and related taxa are as follows:
Clarias liberiensis: 1 specimen (SL = 60 mm):
FMNH 50272 (cleared and stained).
Corxdoras aeneus: 3 specimens (SL = 42-69 mm):
FMNH 54832 (cleared and stained).
Dorascarinatus: 1 specimen (SL = 110mm): FMNH
53192 (cleared and stained).
Helogenes marmoratus: 1 specimen (SL = 60 mm):
FMNH 70115 (cleared and stained).
Ictalurus punctatus: 9 specimens (SL = 160-400
mm): FMNH 16711. 86267. 6430. 63699 (skele-
tons): LU F.082256. F082257. F082258. F.082259.
F082260 (cleared and stained, alcohol).
Ictalurus balsanus: 2 specimens: FMNH 51269 (dis-
articulated skeletons).
Ictalurusfurcatus: 1 specimen: FMNH 73900 (very
large disarticulated skeleton).
Noturusgyrinus: 1 specimen: (SL = 56 mm): FMNH
42269 (cleared and stained).
Rhamdianicaraguensis: 1 specimen: (SL = 150mm):
FMNH 5904 (cleared and stained).
Rhamdia nasuta: 1 specimen: (SL = 75 mm): FMNH
35319 (cleared and stained).
Tramcmh)el:yoFpMteNriHcht6h9y9s29tae(ncilaetaurse:d1ansdpesctiamienned:).(SL 65
Trichomycterus banneaui: 2 specimens: (SL = 65-71
mm): FMNH 70014 (cleared and stained).
Trichomycterus laticeps: 2 specimens: (SL = 38-45
mm): FMNH 79128 (cleared and stained).
Abbreviations
The following abbreviations are used for insti-
tutions and anatomical terminology:
FMNH Field Museum ofNatural History. Chi-
cago
LU
Loyola University. Chicago
UAM
University of Massachusetts. Amherst
act actinotrichia
anp anterior nuchal plate
ar anterior radial (= supraneural of
Grande & Lundberg. 1988: pterygiop-
hore of Fink & Fink. 1996)
boc
basioccipital
br bony ridge
chc chordacentrum (sensu Schultze & Ar-
ratia. 1986)
cl claustrum
dare dorsal arcocentrum {sensu Schultze &
=
Arratia. 1986: basidorsal of Patter-