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Ultrastructure of the turtle spermatozoon.

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THE ANATOMICAL RECORD 229:473-481 (1991)
Ultrastructure of the Turtle Spermatozoon
Department of Veterinary Biosciences, University of Illinois, Urbana, Illinois 61801
(R.A.H.);Poultry Science Department, Clemson University, Clemson, South Carolina
29634-0379 (R.J.T.);Department of Biological Sciences, University of Cincinnati,
Cincinnati, Ohio 45221 -0006 (D.H.G.)
The turtle spermatozoon is vermiform in shape with a narrow
pointed head that is curved. In general, the turtle sperm contains a typical head,
midpiece and tail, similar in morphology to that of birds, amphibians and other
reptiles. However, several structures are unique. These unusual features include
(1)a perforatorial cap over the proximal end of the nucleus, which contains 2-3
rods that are contiguous with intranuclear tubules; (2) a connecting collar of dense
material that surrounds the base of the nucleus; (3) a distal centriole containing
central microtubules that extend its entire length and having outer triplicate
microtubules that open toward the central cavity of the centriole; and (4) unusual
spherical mitochondria containing 7-8 outer laminated membranes.
Male and female reproductive cycles are not synchro- TEM according to Hess et al. (1986).For SEM, a drop of
nized in temperature zone turtles, resulting in the pro- sperm suspended in ethanol was placed on a glass covduction of their respective gametes a t different times of erslip and the sperm were allowed to settle. The samthe year (Licht, 1984). This necessitates a long interval ples were taken through critical point drying in CO,
of gamete survival which is accomplished by the stor- and coated with gold a t 10 pA for 440 sec. Photographs
age of spermatozoa. This storage is thought to occur in were taken with a JEOL 848 SEM. For TEM, the dethe epididymis (Moll, 1979) but may also occur in the hydrated samples were embedded in low viscosity resin
female reproductive tract (Gist and Jones, 1989). Pro- and sectioned. Tannic acid fixation (4% tannic acid in
longed survival of sperm in both the male or female 3% glutaraldehyde) was used for negative staining of
reproductive systems suggests that turtle sperm may microtubules in the distal centriole (Tilney et al.,
possess morphological specializations contributing to 1973). Ultrathin sections were stained with uranyl actheir longevity. Past observations of their ultrastruc- etate and lead citrate and photographed with a JEOL
ture have not revealed organelles unusually different 1OOCX TEM.
from sperm of other species that are capable of longRESULTS
term storage (Miranti et al., 1964; Kaplan et al., 1966;
Furieri, 1970). The basic structure of the turtle sperSpermatozoa of the turtle Chrysemys picta are long
matozoon is well-defined (Furieri, 1970). However, (50-55 pm) and narrow (maximum of 0.9 pm), giving
methods for optimum preservation of tissues must be them a vermiform appearance, with a head that is
used to attain finer resolution of several structures. In curved and pointed (Figs. la-3). Viewed by SEM, bulgparticular, ultrastructures of the globular mitochon- ing spheroidal mitochondria were conspicuous in the
dria, intranuclear tubules, and the distal centriole midpiece (Fig. lb).
should be clarified. Therefore, the purpose of the
present study was to examine the ultrastructural charHead
acteristics of turtle sperm using improved methods of
The head is 11-12 pm long by 0.9 pm wide at the
fixation and staining. We report the sperm ultrastruc- largest diameter. The tapering anterior one-third of
ture of a species (Chrysemys picta) in which oviductal the acrosome extending beyond the tip of the nucleus
sperm storage may be a n essential component of the has a dense homogeneous matrix that continues postereproductive cycle (Gist et al., 1990).
riorly in a very thin layer that covers the perforatorium and the anterior protrusion of the nucleus (Figs.
2,4,5). The acrosomal membrane is separated from the
Turtles (C. picta) were captured in October 1988 from overlying plasmalemma by a space of varying width
ponds located in southwestern Ohio. Sperm was col- (Figs. 6-8). At the posterior margin of the acrosome,
lected within one week of capture by cloaca1 electro- the plasmalemma is very closely bound to the outer
ejaculation a s described elsewhere (Gist et al., 1990) nuclear membrane, forming a junction that closes off
and suspended in physiological saline. Spermatozoa the subplasmalemmal space over the anterior portion
were concentrated by centrifugation and resuspended of the head (Fig. 5). In the subacrosomal area, a thin
in 3% glutaraldehyde (in 0.1 M cacodylate buffer, pH
7.4) and fixed for 3 hr. After 3 washes in cacodylate
buffer, the samples were postfixed in 1% osmium
tetroxide for 1 hr. After dehydration through a graded
Received November 16, 1989; accepted September 25, 1990
ethanol series, the samples were processed for SEM or
lntranuclear Tubule
Connecting Piece
Proximal Centriole
Distal Centriole
Outer Dense Fibers
Fibrous Sheath
Fig. 1. a: Illustration of the turtle spermatozoon. b SEM of the head, midpiece and proximal region of
the principal piece of the tail. Bar = 1 pm.
space separates the acrosomal cap from the perforatorium (Figs. 5, 8).
The perforatorium consists of two components: (I) a
central core of 2-3 electron-dense rods covered by a
thin membrane (Figs. 4, 71, and (2) a n outer granular
material t h a t covers the thin anterior portion of the
nucleus (Figs. 4-5, 8). The electron-dense rods appear
continuous with the dense cores of the intranuclear
tubules and extend from the nucleus to the subacrosoma1 space at the tip of the perforatorium (Fig. 4). Beginning at the terminus of the acrosomal cap, the nucleus tapers as it penetrates the dense granular
material of the perforatorium (Figs. 2,5). The nucleus
ends a t the point where the rods of the perforatorium
are continuous with the nuclear tubules (Fig. 4).
The nucleus contains intensely stained chromatin
surrounded by a n adherent membrane (Figs. 2, 5, 10).
Paired or occasionally triplicate tubules, 55 pm in diameter and outlined by the nuclear membrane, extend
through the center of the nucleus for approximately
three-fourths of the length of the nucleus (Figs. 2, 8, 9,
11).I n the anterior portion, these tubules contain a
dense core, triangular-shaped in cross section (Fig. 9);
but at the terminal end the interior is electron lucent
(Figs. 8, 11).
Connecting and Middle Pieces
A cross-striated connecting piece terminates in a
concave implanlation fossa in the caudal end of the
nucleus (Figs. 12-15). A connecting collar of finegrained amorphous material is wedged between the
first mitochondria and the base of the nucleus (Fig. 12).
This material extends laterally and upward while tapering to a point and forming a circumferential collar
around the nucleus (Figs. 12, 14-15). When the spermatozoa were sectioned with proper orientation, a
proximal centriole perpendicular to the distal centriole
could be observed inserted into a vault of the connecting piece (Figs. 12, 13).
The midpiece consists of proximal and distal centrioles surrounded by mitochondria (Fig. 12; see Fig. 19).
A well-defined annulus separates the midpiece from
the tail (see Fig. 19). A majority of spermatozoa taken
from the epididymis, and a few from the ejaculate, contained a midpiece cytoplasmic droplet consisting of
lipid-like bodies, vacuoles and smooth membranes (described in a separate article; Gist et al., submitted).
The centrioles consist of typical nine triplet microtubules arranged in a pinwheel fashion and surrounded
by a dense material (Figs. 16, 17). Triplicate microtubules of the distal centriole extend caudally through
approximately two-thirds of the midpiece. In the anterior portion of the midpiece, a dense matrix forms a
ring around the distal centriole and permeates the
space between the microtubules (Fig. 16b). Moving
caudally along the centriole, radial links project from
this outer dense material, forming spaces between the
sets of triplicate microtubules to join dense material
surrounding the 2 central microtubules (Fig. 16a,c).
Dissolution of the radial links occurs in distal progression (Fig. 17). Finally, only remnants of the dense substance remain attached to each of the outer nine doublets and the central singlet microtubules (Fig. 18).
This outer dense fibrous material was lost in the prin-
cipal piece of the tail, leaving only well-defined axonema1 units (see Figs. 21, 22).
With routine electron microscopic staining, the distal centriole appears to contain doublet microtubules
enmeshed by the dense outer ring of matter (Figs. 16a,
17a). With negative staining, the C microtubule of the
triplicate is clearly seen (Figs. 16b, 17b). However,
within a short distance from its origin, the C microtubule is open to the central axis, forming a longitudinal
The mitochondria of turtle sperm form 5 rows of 10
spherical bodies each for a total of 50 mitochondria per
spermatozoon (Figs. 12, 16-18). They possess a n unusual structure. The core consists of thick-walled tubular cristae. Surrounding this mitochondria1 core are
7-8 concentric membranes, apparently lipid bilayers
(Figs. 16-18). Lucent channels form the interior of the
dense branching cristae (Figs. 16-18). The thick outer
wall of the core forms a projection to which the concentric membranes are attached (Fig. 18a). The lamination (18 nm in width) preferentially binds lead citrate,
creating a peppered appearance with clear spaces between layers (Figs. 17, 18). The plasmalemma of the
mid-piece may be directly adjacent to the mitochondria
or separated from them by a thin layer of cytoplasm
(Figs 12, 16-19). In some areas, this layer is expanded
as a n eccentric droplet of residual cytoplasm.
Principal and End Pieces of the Tail
The nxoncmal complex of the principal piece of the
tail is surrounded by several layers of dense granular
material of the circumferential fibers (Figs. 19-21).
Near the annulus, these fibers are 24 nm in diameter,
and several layers thick (Fig. 19), but they are reduced
to a single layer near the endpiece (Fig. 20). A finegrained material, covered by the plasmalemma, surrounds the circumferential fibers at the beginning of
the principal piece (Fig. 19), but this material stops at
the beginning of the endpiece of the flagellum, which
consists of the axonemal complex surrounded only by
the plasmalemma (Figs. 20, 22). The A microtubule of
the axonemal doublets begins to lose its dense core
while still in the principal piece. Near the end of the
flagellum, the doublet microtubules appear as singlet
tubules with lucent cores and eventually their axonema1 organization is also lost (Figs. 22, 23). Out of 15
cross sections of the terminal end piece, 4 contained 20
singlet microtubules (Fig. 23), while others exhibited
6-19 microtubules.
The sauropsid form of the turtle sperm is similar to
that of domestic birds, amphibia and other reptiles.
However, several structures are unique from what is
seen in mammalian and even other reptilian spermatozoa (Afzelius, 1979; Asa e t al., 1986; Boisson and
Mattei, 1966; Burgos and Fawcett, 1956; Butler and
Gabri, 1984; Carrick and Hughes, 1982; Clark, 1967;
Fawcett, 1970; Philips and Asa, 1989; Picheral, 1979;
Thurston and Hess, 1987). These unusual features include (1)a perforatorial cap over the proximal end of
the nucleus, which contains 2-3 rods that are contiguous with intranuclear tubules; (2) a connecting collar
of dense material that surrounds the base of the nucleus; (3) a distal centriole containing central microtu-
Figs. 2-10
proximal centriole and extends into the implantation
fossa at the base of the nucleus. Furieri (1970) did not
separate the connecting piece from the surrounding
collar and reported transverse microtubules outlining
this piece. We did not find these microtubules; therefore, it is possible that the fixation method used in the
earlier work (osmium tetroxide as the primary fixative) induced artifacts. In sperm from several avian
species, a nonbanded connecting material projects from
the triplicate, centriolar microtubules and inserts into
the base of the nucleus (Asa et al., 1986; Thurston and
Hess, 1987; Phillips and Asa, 1989). The connecting
piece of mammalian sperm contains a capitulum located anterior to the centriole (Fawcett, 1970).
As in the lizard (Clark, 1967), the toad (Burgos and
Fawcett, 19561, and the bird (Thurston and Hess,
1987), turtle sperm contain 2 centrioles, the proximal
centriole a t a right angle to the distal. However, the
distal centriole in the turtle sperm has 2 central microtubules as in the rhea bird (Phillips and Asa, 19891,
rather than a lucent core as in amphibians (Burgos and
Fawcett, 19561, lizards (Clark, 19561, nonpasserine
birds (Thurston and Hess, 1987), and the more primitive tinamou bird (Asa et al., 1986). Furieri (1970) reported, without illustration, that the turtle sperm contains a distal centriole but also claimed that the
anterior portion of this structure was not a centriole.
He reported that the opaque material that wraps the
anterior portion of the flagellum forms a space alongside the doublet microtubules, giving the appearance of
a third microtubule, as in a centriole. In the present
study, tannic acid negative staining demonstrated that
a third microtubule is present and that this microtubule forms a unique opening along its inner longitudiFig. 2. Acrosomal cap (A) covering the subacrosomal perforatorium
nal side. Although it is well established that in cross
(P) and twisted intranuclear tubules (T) that pass through the center
section the B and C microtubules form partial rings
of the nucleus (Nu). X 26,000.
(the B ring bound to the A microtubule, and the C ring
Fig. 3. The apex of the acrosome (A) is homogenous, consisting of
bound to the B microtubule; Dustin, 1984), to our
fine-grained, amorphous material anterior to the perforatorium (P). knowledge this is the first report of a microtubule
PI, plasmalemma. x 45,000.
groove being formed by a space between the protofilaments of the B and C microtubules.
Fig. 4. The dense material that surrounds a perforatorial rod (R)
may be part of the perforatorium. The rod is continuous with the
The mitochondria have unusual configurations and
contents of an intranuclear tubule (TI. A, lateral extension of the form poorly defined, but thick, dense cristae cores, suracrosomal cap; S, lucent space between granular material of subacrounded by concentric layers of membranes. The mitorosomal components and the outer acrosomal cap. X 45,000.
chondria assume a staggered rows-and-columns arFig. 5. A junction (J) is formed by the adherence of the plasmarangement (10 rows and 5 columns) around the distal
lemma (PI)to the nuclear membranes at the base of the acrosomal cap centriole, rather than a helix as in mammalian (Faw(A). The dense granular material of the perforatorium (P)terminates
cett, 1975) and avian sperm (Thurston and Hess, 1987).
at the junction (*I. T, intranuclear tubule; Nu, nucleus. x 69,000.
Mitochondria from invertebrates display peculiar
Fig. 6. Cross section of sperm head (level 6, Fig. 3) illustrates hoshapes (ring-shaped, fused, and triangulated; Afzelius,
mogeneity of the anterior region of the acrosomal cap (A). The cap is
1979), and Chinese hamster sperm have circumferensurrounded by a swollen plasmalemma (PI). x 45,000.
tial cristae (Fawcett, 1970). Opossum spermatozoa
have spirals of membranes within the mitochondria1
Fig. 7. Cross section of a sperm head (level 7, Fig.-4) depicting
circumferential acrosomal cap (A), perforatorial granular material (P) core (Fawcett, 1970) and membranous configurations
and rods (R). X 45,000.
are seen in mitochondria of the rhea (Phillips and Asa,
1989). However, no comparable structure such as the
Fig. 8. Cross section of nucleus (Nu; level 8, Fig. 5) with two intranuclear tubules (T) containing triangular dense material. A, acroso- lipid bilayers of turtle sperm has been identified in
ma1 cap; P, granular material of the perforatorium; Nu, nucleus.
sperm from other species. Mitochondria1 modifications
x 45,000.
are reported in other species such as the bat, in which
sperm also overwinter in the female tract (Wimsatt et
Fig. 9. High magnification cross section in the apex of the nucleus
al., 1966; Uchida and Mori, 1972) but are unlike those
(Nu). The intranuclear tubules are outlined by membranes with 910-nm particles dotting the surface (arrows). x 104,000.
of the turtle. Under appropriate conditions, mammalian spermatozoa can use phospholipids as a n energy
Fig. 10. Cross section in the caudal region of the nucleus (level 10,
Fig. 11)showing a single intranuclear tubule (T)surrounded by dense source (Mann, 1966); thus, we speculate that the unusual laminated mitochondria of turtle sperm might
chromatin. x 45,000.
bules that extend its entire length and having a outer
triplicate microtubules that open toward the central
cavity of the centriole; and (4) unusual spherical mitochondria containing 7-8 outer laminated membranes.
The head of the turtle sperm is vermiform in shape
rather than lance-shaped as described by Furieri
(1970). Its acrosome forms a single cap as seen in many
avian and mammalian sperm (Fawcett, 1970;Thurston
and Hess, 1987). However, the subacrosomal space contains a perforatorium, not a second coaxial cap (Furieri, 1970), that differs considerably from those of
other species. The perforatorium consists of rods surrounded by a granular material that forms a cap over
the apex of the nucleus. This general structure resembles the perforatorium of lizard sperm (Butler and
Gabri, 1984; Clark, 1967; Da Cruz-Landim and Da
Cruz-Hofling, 1977; Del Conte, 1976) and those of amphibians (Burgos and Fawcett, 1956; Picheral, 1979)
more than the perforatorium of avian sperm (Asa et al.,
1986; Thurston and Hess, 1987).Like the rhea (Phillips
and Asa 1989) and crested tinamou (Asa et al., 1986),
the nucleus of the turtle sperm contains tubules, but
they are unique in having a dense core and being lined
by nuclear membranes (Sprando and Russell, 1988;Yasuzumi and Yasuda, 1968).
The connecting piece of turtle sperm consists of alternating light and dense bands formed anterior to the
Fig. 11. Longitudinal section through the nucleus. Tubules (T)
extend longitudinally through the center of the nucleus for at least
the anterior two-thirds of the nucleus. Nm, nuclear membrane, P1,
plasmalemma. x 38,000.
Fig. 12. Longitudinal section through the midpiece. The base of the
nucleus (Nu) forms a n implantation fossa (14)into which is inserted
the banded connecting piece (15)of the neck. A connecting collar (Cc)
surrounds the nucleus. Dense material of the collar is continuous with
the dense matter of the proximal (Pc) and distal centrioles (16). The
spherical, laminated mitochondria (M) are aligned in columns around
the centrioles. Outer dense fibers (18)of the axoneme are continuous
with the dense regions of the distal centriole. The principal piece of
the tail contains a circumferential fibrous sheath (Cf). The numbers
function to sustain the sperm during the long storage
in the female oviduct.
Prominent outer dense fibers are attached to the
outer doublet microtubules in the midpiece of turtle
indicate levels for approximate cross sections shown in subsequent
figures. An, annulus; L, lipid droplet. x 26,000.
Fig. 13. High magnification of the neck region. Note the proximal
centriole (Pc) in a vault of the connecting piece (Cp). Cc, connecting
collar; Dc, distal centriole; M, mitochondria; Nu, nucleus. x 40,000.
Fig. 14. Cross section of the nucleus (level 14, Fig. 12). The connecting collar (Cc) extends completely around the nucleus (Nu). 1, lucent
area marking the beginning of the implantation fossa. x 45,000.
Fig. 15. Cross section of the neck (level 15, Fig. 12). A portion of the
connecting piece (Cp), nucleus (Nu), and connecting collar (Cc) is depicted. x 45,000.
sperm. These structures are absent or reduced in birds
(Thurston and Hess, 1987; Phillips and Asa, 1989) but
become pronounced in mammalian sperm (Fawcett,
1975).Thus, it may be argued evolutionarily that these
Fig. 16.a: Cross section of midpiece (level 16; Fig. 12) illustrates
the electron dense matrix (Dm) surrounding the anterior portion of
the distal centriole. Dense material surrounds the central singlet
(Cm) and outer triplet (Tm) microtubules and forms radial links between the outer ring and the inner matrix. Five columns of mitochondria (M) surround the distal centriole in the midpiece. x 55,000. b
Tannic acid negative staining of a n anterior region of the distal centriole. The triplicate microtubules (a-c) are completely surrounded by
the dense matrix (Dm). The b and c microtubules form partial rings
that do not open to the matrix. Two central microtubules are also
present in the anterior region. x 90,000. c: Tannic acid negative staining of the distal centriole in a region similar to a. The triplicate
microtubules are present (a,b,c) but the “c” microtubule opens to the
inside and forms a space within the dense matrix (arrow). x 90,000.
Fig. 17.a: Cross section of midpiece (level 17, Fig. 12) showing the
characteristic dissolution of dense matrix in the caudal portion of the
distal centriole. The dense matrix forms incomplete radial spokes
near the central microtubules (Cm). Tm, outer triplet microtubules;
M, dense matrix of a mitochondrial core. x 55,000. b: Tannic acid
negative staining of the caudal region of the distal centriole. The
central space that is continuous with the c microtubule (arrow) nearly
surrounds the two central microtubules. a-c: Triplicate microtubules.
x 90,000.
Fig. 18.a: Cross section of midpiece (level 18, Fig. 12). At this level,
the dense matrix remains as outer dense fibers (Odf) associated with
the outer doublet microtubules (Dm). The dense matrix nearly obscures the a microtubules. The dense wall of the mitochondrial cristae
(Mc) protrudes to one side, to which the lamellar membranes are
attached (*). The laminated membranes (La), which are layered over
the mitochondrial core, are preferentially stained with lead citrate.
Cm, central microtubules. x 55,000. b The beginning axonemal complex at level 18, Figure 12. The outer dense fibers (Odf) mask the a
microtubules but both a and b microtubules are revealed with tannic
acid negative staining. x 90,000.
Fig. 19. Longitudinal section of the midpiece-tail junction. A
wedge-shaped annulus (An) separates the last mitochondria (M) and
the principal piece. Outer dense fibers (Odf) of the axoneme continue
for a short distance into the principal piece where a thick layer of
circumferential fibers (Cf) form a sheath around the axonemal complex. Cm, central microtubules. X 52,000.
Fig. 20. Longitudinal section of the junction between the principal
and end pieces of the sperm tail. The circumferential fibers (Cf) are
still present in the principal piece but are reduced in thickness. Central microtubules (Cm) are linked by a bridging substance (B). Dm,
outer doublet microtubules. X 52,000.
fibers developed early in vertebrate species, were lost
in modern birds but then retained in the line leading to
mammals. The circumferential fibrous sheath of the
turtle sperm is similar to that in the rhea bird (Phillips
and Asa, 1989) and the Platypus (Carrick and Hughes,
1982). However, the longitudinal thick columns of fibers that are prominent in mammalian sperm are absent in the turtle (Fawcett, 1970).
Fig. 21. Cross sections of the principal piece reveal multiple and
single layers of the circumferential fibers (Cf) woven around the axoneme. The axonemal complex consists of (A) and (B) microtubules,
dynein arms (D) and radial links (Rl). In some doublets, the a microtubule has a lucent core. x 52,000.
Fig. 22. Cross section of the endpiece of the tail. Only the plasmalemma surrounds the axoneme a t this level. X 52,000.
Fig. 23. Cross section of the endpiece illustrating the dissociation of
the axonemal pattern into 20 singlet microtubules. x 52,000.
The flagellum exhibits a typical configuration of 9 +
2 microtubules common to avian and mammalian
sperm (Fawcett, 1970; Thurston and Hess, 1987). The
doublet microtubules became single near the tip of the
flagellum, which produces up to 20 singlet microtubules in cross section, as it occurs in some mammalian
species (Woolley and Nickels, 1985). However, the
dense core of the A microtubule, which is normally lost
after the formation of single tubules in the endpiece
(Woolley and Nickels, 1985),begins to lose its electron
density in the principal piece.
The turtle sperm contains several unique structures
whose evolutionary origin and functional significance
are intriguing. Of particular interest for future study is
the function of the perforatorium, the intranuclear tubules, and the laminated mitochondria.
We are grateful to Lou Ann Miller, of the Veterinary
Medicine Electron Microscopy Suite, for outstanding
technical assistance, and to the Spring Lawn Association, Cincinnati, Ohio, for the use of their ponds.
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ultrastructure, turtles, spermatozoa
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