Walking versus breathing: mechanical differentiation of sea urchin podia corresponds to functional specialization

6 Pages·2000·2 MB·English

by  H A Leddy

Reference: Bio/. Bull. 198: 88-93. (February 2000)
\Yalking Versus Kreathing: Mechanical Differentiation
of Sea Urchin Podia Corresponds to
Functional
Specialization
HOLLY A. LEDDY1'* AND AMY S. JOHNSON
v l)cpaninein, Bowdoin College. Brunswick, Maine 04011
,'
\hstruct. The podia of sea urchins function in locomo- double rows of podia, and these structures are essentially
tion, adhesion. (ceding, and respiration; but different podia hollow lubes with terminal suckers. The wall of each po-
on a single urchin arc often spcciali/cd to one or more of dium consists of three main layers: an outer epithelium, a
these tasks. \Ve examined the morphology and material middle connective tissue layer, and an inner muscular layer
properties of podia of the green sea urchin. Stron^yloccn- (Florey and Cahill. 1977). Internally, the podium is con-
irotns Jri>chucliicii.\i.\. to determine whether, despite appar- necled to an ampulla, a sac-like structure that antagoni/es
ent similarities, they achieve functional speciali/ation along podial movement. Contraction of the ampulla forces coelo-
the oral-ahoral axis through the differentiation of distinct mic thud into the podium, and thus extends it. Conversely,
mechanical properties. We found that oral podia, which are contraction ofthe longitudinal muscles shortens the podium
used primarily for locomotion and adhesion, arc stronger and forces coelomic fluid back into the ampulla. All of the
and thicker than ahoral podia, which arc used primarily for podia on S. droebachiensis share these characteristics, and
capturing drift material and as a respiratory surface. The all ofthem are similarly shaped. They exemplify the typical
functional role of ambitul podia is more ambiguous: how- echinoid locomotory podia.
ever, they are longer and are extended at a lower strain rate However, podia perform a variety of functions besides
ili.in other podial types. They are also stronger and stiller locomotion, including adhesion, feeding, shading, sensing,
than aboral podia. In addition, all podia become stronger and respiration, and many podia are speciali/ed for one of
and stiffen when extended at faster strain rates, in some these functions. I'odia in a particular position along the
cases by nearly an order of magnitude for an order of oral-aboral axis lend lo perform a particular function and
magnitude change in strain rate. This strain-rale dependence often exhibit morphological features thai enhance pertor-
implies that resistance to rapid loading such as thai imposed mancc of (hat function. Lor example. Arhacia /nincliilatd
by waves is high compared to resistance to slower, sell- has morphologically differentiated podia, reflecting the sep-
miposcd loads. Thus, the serially arranged podia ol'S. ili'nc- aration of respiratory, sensory, and locomotory functions.
hachiensix are functionally speciali/ed along an oral-aboral The aboral podia lack suckers and their larger surface area
axis by differences in (heir morphology and mechanical and thinner walls enhance respiration, (he ambital podia are
properties. long with minimal suckers to allow sensation in ihe region
around (he urchin, and the oral podia are suckered to facil-
Introduction itate locomotion (L'enner. 1973).
The surface of the green sea urchin, Strongylocentrotus Although the podia ofS. droebachiensis lack these gross
(ln>ehcichiensi\. like that ofall urchins, is covered with live morphological differences, there may still be a division of
labor between the primarily locomotory oral podia and the
We
primarily respiratory aboral podia. hypothesi/e thai the
R'ePcreeisevnetdA2d1drOecstsobe.r I'm.I.Kxpc.iprticidncnIl.XDNuokveemUbneivrerlsity. Durham. NC ptohdrioaughoftheIhdiisffesrpeenctiieatsionacohfiedivseiinfcutncmteicohnaanlicsaplecpiraolpie/rattiieso.n
27708.
* Authorlowhom conx-.poiuh-ni.-e should he addressed. E-mail: ha!2l" The goal of this study was to icsi our hypothesis thai the
acpub.dukc.edu differences in function oforal, aboral. and ambital podia are
MECHANICAL SPECIALIZATION OF PODIA 89
correlated with differences in their mechanical characteris- In comparing lengths ofdifferent podial types and calcu-
tics and morphology. lating strain and strain rate, initial length of the podium
(measured between the body wall and the end of the clip)
Materials and Methods was defined as the point at which force started to increase
(above 0.001 N) during the breaking tests, thus indicating
Sea urchins. Stronglyocentrotus droebachiensis, were thatthe podium hasjust started to stretch (Fig. la). Nominal
caonlilmeacltse,drsaunbgtiindgalliny dnieaamretMeronfhreogman45.I4slmanmd. tMoai5n9e.7. mTmh,e satprpelsisedonbyathpeodmieuamn wtiasssuecaclrcouslsa-tseedctbiyonadlivairdeiangoftpheodifoarcoef
were maintained in a recirculating seawater aquarium kept that type from that urchin. Nominal strength is the nominal
at 1()C and fed Laminaria sp. every 2 weeks. stress at which a material breaks. True strain was calculated
by taking the natural logarithm of the length divided by the
Natural extension initial length. Stiffness is the slope of a stress-strain curve
Urchins in a glass aquarium were videotaped, and the and was taken from the upper, linearportion ofthe J-shaped
natural extension rate and initial length of podia were mea- stress-strain curves (Fig. Ib). Strain rate was calculated by
sured from the digitized video images. The length of a dividing the final strain by the time required to get from
podium was measured from the base to the sucker as it was initial length to breaking.
extending, and just as the podium straightened. Extension
Tissue cross-sectional area
rate was quantified as the increase in length (in millimeters)
per second, and strain rate was quantified as true strain (the Relaxed podia from urchins soaked in 7.5% MgCK
natural logarithm ofthe ratiooffinal length to initial length) 6H,0 were cut off at the base. Although this technique
divided by the time to extend. depressurized the podia, it allowed us to compare the three
types in as similar a state as possible. The exterior and
Mechanical extension lumenal diameters of the podia were measured halfway
between the base and the sucker with an ocular micrometer
Podia from three locations on the animal were tested (0.01 mm) on a light microscope. These diameters were
separately: aboral podia are those on the upper surface of used tocalculate the total and lumenal cross-sectional areas,
the urchin; ambital podia are those occupying a narrow and the tissue cross-sectional area was found by subtracting
circumferential band at the widest diameter of the urchin; the lumenal cross-sectional area from the total cross-sec-
and oral podia are those on the lower surface of the ur- tional area. Five podia ofeach type were measured on each
chin. Urchins were placed in an isotonic solution. 7.59r
urchin.
MgCK 6H^O, at 10C, for 15 min prior to mechanical tests
oftheir podia and were kept in this solution during the tests Results
(Dales. 1970). The MgCl2 solution prevented muscle con-
traction, so passive material properties could be tested. Structure and natural extension
All mechanical tests were performed with an Instron All oral, ambital. and aboral podia had the same gross
material testing device (Model 4301) that loaded materials morphology (suckered tube) and similar diameters (Table
aetxtsepnesciiofni.edForracteesaannddexstiemnuslitoannesoiugsnlaylsmweearseurdeidgitfiozrecde (a1n2d- a1b).orTahleaanmdbiortaallppooddiiaa,,ahnodwetvheer,orawlerpeod6ia7%haldontgheirckterhawnaltlhse
befioxtrt)ceeantsim1oe0na0s0mueHraezsmuaernnedtmsernetcwosarswdead<s0i<n.0a0.0c0o1m1puNmt.emr.T.hTTeehsetesrerrworerorreiinncottnhh-ee atthhneediraabomroarula,clhamogbrrietaaamtlbe,irtacanrldosapsbo-osdreiacalti(poTonaadblilaaeraet1a)t.hoefUstricashmsiuenesrtahteea.xntNeeointndheee-dr
ducted as follows. An urchin was strapped in place, and a theless, because the ambital podia had the greatest initial
small, spring-loaded clip was attached to the distal end ofa length, they also had the lowest strain rate (Table 1 ).
podium. The podium was then pulled perpendicular to the
surface of the urchin (in the direction of normal extension) Mechanical extension tests
at a constant extension rate until it broke.
Fifteen podia 5 aboral. 5 ambital, and 5 oral were All the material properties of all podia were positively
tested on each urchin at agiven extension rate. Each offive dependent on strain-rate (Fig. 2, linear regression analysis,
urchins were tested at three extension rates: 0.167 mm/s all P < 0.05. all d.f. = 86). For the three podial types, the
(minimum natural extension rate). 0.708 mm/s (halfway slopes of breaking force, nominal strength, and breaking
between the mean and the minimum natural extension strain with respect to strain rate were not significantly
rates), and 1.25 mm/s (mean natural extension rate). An- different (ANCOVA. Table 2). For breaking force and
other set of podia from one urchin was also tested at 3.45 nominal strength, the r of the regressions ranged between
r
mm/s (maximum natural extension rate). 0.44 and 0.58; and for breaking strain, the of the regres-
"' H. A. LbDDY AND A. S. JOHNSON
a. b.
0.07 0.6-
Nominal
0.06- <N Strength "
E 0.5
0.05- A stress
=Stiffness
Z 0.4 H Astrain
0.04
o
0.03- & 0-3 H
0.02- S 0.2-
o
0.01
0.
0.00
2 4 6 B 10 12 14 16
[< AL > 0.0 0.2 0.4 0.6 0.8 1.0 1.2
Extension (mm) Strain
Fijjurc 1. Force extension lai and stress-strain (hi cuncs ol an otal podium /,,,. the initial length, is the
length .it which the podium st.irts icsistmg extension; A-,,lk is the lorce at which the podium breaks, and A/, is
the change in length Mom /,, tothe breaking force. Nominal stress is tour dmded h\ cross-sectional area, and
strainisthenatural logarithmof(he lengthdmdedbythe initial length. Stillnessi.stheslopeofthelinearportion
ol this curve. Nominal strength is the stress at which the podium broke, and Slrain,,,k is the siiam .it which the
podium bioke. Inset shows an urchin in the testing setup with one of its oral podia being extended.
sions ranged between 0.(W and 0.13. Thus, although nearly In contrast to the analysis ofother material properties, the
halfofthe variation in breaking force and nominal strength ANCOVA for nominal stiffness revealed significant differ-
is explained by variation in strain rate, little ofthe variation ences between slopes (Table 2). In an ANCOVA. when the
in breaking strain ( r/-l.V;) is explained by variation in slopes of the lines are unequal, comparisons of ele\ations
strain rate. A posteriori comparisons of elevations using cannot be generali/ed across all variations m the indepen-
"lukey's Q (Table 2) revealed that oral podia exhibited dent variable (in this case strain rate). Specifically. <; pos-
higher breaking forces, nominal strengths, and breaking teriori comparisons ofslopes using Tukey's Q revealed that
strains than aboral podia: i.e.. the oral podia were stronger oral podia exhibited less positive strain-rate dependence
and stretchier. The ambital podia also exhibited lower than did amhilal podia. For those comparisons showing no
breaking forces and breaking strains than did the oral podia. significant difference between slopes, we found that ambital
but they were equally sirong. podia were significantly stifferthan aboral podia at all strain
I:ihli- I
iiii'iiilinliii>\
MECHANICAL SPECIALIZATION OF PODIA 91
a. c.
4.0
0.1-
.S
a
en
60
C(0Q81j i1 - |irD nH,"Qu w- vvC
CQ fl
0.01- _* n^ nn
0.4
0.01 0.1 0.01 0.1
Strain Rate (s-i) Strain Rate (s-1)
b. d.
-
i
g
S
2 2
i in 1-
en
01
I
CD CD
lo,
& z ai
ffi
0.01 0.1 0.01 0.1
Strain Rate (s-1) Strain Rate i
Figure2. Breaking force(a), nominal strength(b).breaking strain (c). and nominal stiffness(d)are plotted
onalog-logscaleagainststrain ratefororal(crosses,dottedline),ambitul(filledcircles,dashedline),andaboral
(open squares, solid line) podia. Lines are least-squares linear regressions. Line slopes and elevations were
ANCOVA
compared by (Table 2).
rates, and aboral podia were significantly stiffer than oral droebachiensis, that live in high-flow environments, may
r
podia at all strain rates; values for these regressions require suckered aboral podiatosecurethemselves incracks
ranged from 0.30 to 0.43. and to right themselves (Fenner, 1973). Thus, aboral podia,
though performing a different set of tasks from oral podia,
Discussion would still require the same gross morphology.
Some ofthe morphological differences found among the Although all podia in S. droebachiensis do possess suck-
podia of other urchins (e.g., presence versus absence of ers, they still exhibit mechanical and morphological differ-
suckers) are absent in Strongylocentrotus droebachiensis, entiation consistent with their location and functional spe-
possibly because the aboral podia, in addition to acting as a cialization for locomotion or respiration. The greater
respiratory surface, perform other functions that require strength and thicker walls of the oral podia presumably
suckers. For example, drift algae captured by aboral podia enhance one of their primary functions, which is to resist
may be the primary food source for some urchins (De hydrodynamically generated forces on the urchin (Denny
Ridder and Lawrence, 1982). Furthermore, urchins like S. and Gaylord, 1996). Similarly, the thin walls of the aboral
92 H. A. LEDDY AND A. S. JOHNSON
Tahli- 2 would resist faster, hydrodynamically generated loads. Sim-
Comparison ofstrain-raledependentmaterialprn/>: ilarly. Koehl ( 1977) found that the body wall of sea anem-
ones exhibited greater resistance to rapid loads, such as
Material property IN.Ml ,'t elevations those imposed by waves, than to slower loads, such as
> self-imposed forces that function to expand their body.
(1i21;))i NBBrroeemaaikkniiannlggsfsttorrreacniengt(hN)(N mm":) (iOrpia.ill = aliamnibinihbititatalall)>=aaabbbooorrraaalll) in Imnaanybrooatdheerr csotnrtuecxttu,remsecchonasntircuaclteddiffoefresnetriiaatlliyonairsrfaonugnedd
(4) Nominal stiffness(N mm~:i Ambital > aboral building blocks in both invertebrates and vertebrates. For
Aboral >oral example, crinoids reorient passively in flow through varia-
Comparisons of uta shown in Figure 2. For material tion in the stiffnessofthe collagen in thejoints oftheirstalk
properties (1-3). si not statistically different from each other (Wilkie i-1 nl.. 1993). Also, intervertebral joints in both
(ANCOVA.P>0.05.u.l = 2.259),soallcomparisonsofelevationsweim- dolphin (Long et al.. 1997) anil blue marlin (Long. 1992)
possible. For nominal stiffness (4). a posteriori statistical analysis by exhibit regional mechanical speciali/ation that enhances
coTamuniktteltyye'ds:difaQfllerroeetnhteri/'sl<opne0.su.0w5se.lroedp.efss.taf=toirst3iu.cmab2lil5yt9a).lsimaainnlddarsooriaTluthkapeioyd'cisoamQpw.aerrPies>osnig0m.wl0ai5s-. smawriimlmyionngmpeecrhfaonrimcaanlced.ifTfhereesnetiadtiivoenrsteosetnrhucatnucreesthreeilry pperri--
= ANCOVA formance.
d.f. 3.259).Overall forelevations\vasalwayssignificant (all
P < 0.05. all d.f. = 2. 261). Symbols indicate results ol u /),<w,-n,in From arthropod segments and appendages to mammalian
statistical analyses by Tuke\\ (J i/' (1.05. d.f. = .V 259). where ": vertebrae and teeth, this regional speciali/ation ofrepeating
means "not significantly different" and '" means "sigmticanlly greater units has arisen many times. Division of labor by regional
than." speciali/ation can increase efficiency by not sacrificing per-
formance to maintain multiple conflicting functions, and
podia, as well as their greater exposure to flow, are well- serially homologous structures provide a model system in
suited to facilitating gas exchange (Fenner. 1973). The which to examine the evolutionary conflicts between func-
intermediate position ofumbital podia combined with their tional design and developmental constraints (Wilson and
greater length and thinner walls may allow them to function Hoyle. 197S).
in both oral and aboral capacities: however, a distinct func- Mechanical speciali/ation can arise from differences in
tional role for amhiial podia has not yet been determined. morphology or from differences in material properties of
These podial differences arise from differences in both tissues. For example, mechanical speciali/ation of interver-
morphology and material properties. Because the oral and tebral joints may result from differences in the morphology
amhital podia have equal tissue strength, the greater break- of the surrounding vertebrae and from differences in the
ing force of oral podia results solely from a greater cross- material properties of the interxertebral disk (Long. 1992).
sectional area. In contrast, the low breaking force of aboral Fven when morphological differences have not been de-
podia relative to ambital podia is a result of their lower tected, mechanical differentiation can play an integral role
tissue strength, because the cmss-seclional areas of these in enhancing or differentiating performance.
two podial types do not differ from each other. Such dif-
ferences in tissue strength may he due to line-scale variation Acknowledgments
in morphology (e.g., collagen fiber orientation) or tissue
composition (e.g.. proportion of muscle relative to connec- fins work would no! have been possible without ilk-
tive tissue). ideas, insight, and comments of O. Ellers and C. K. John-
All the material properties, especially strength and stiff- son. Thanks to H. Archie. Z. Cardon. P. Dickinson, and M.
ness, varied positively with strain-rate over the range of Pratt for (heir insightful comments on the thesis version of
natural extension rales observed. In some cases, there was (his work and to C. Fuller for urchins. Thanks also to three
nearly an order of magnitude increase in silliness or anonymous reviewers for many helpful comments. This
strenglh lor an order of magnitude increase in strain rale. work was supported by a SURDNA Undergraduate Re-
The consequence of this strain-rate dependence to the per- search Foundation Fellowship to H.A.I..
formance of a given podium is that slow extensions requite
lessenergy than do rapid extensions, For a gi\en strain rate, Literature Cited
amhital podu require more energy to extend, hut because Ikilcs, R. IV 1970. Practical Inverlehrate Zoology University of Wash-
they are extended al lower strain rales, it is unclear whether ington Press. Seattle.
there are energetic 'iil'tcrences in the urchin's own use of Drum. M., nitd II. i..i\l.ini 1996. Why the urchin lost its spines:
different types ol hydroilynamic forcesand survivorship in threeechinoids.7. /:.v/>. liiol.
| 199(3): 717-729.
II the strain-rate d< , we quantified extends to the IK- KI.I.I. i ('., and J. M. l.awri'tiiT. 1982. Food and feeding mecha-
range ofstrain rates applied by \\a\es, then this mechanical nisms: Kchmoidea. Pp. 57-115 in Echinoderm Nutrition, M. Jangoux
difference would facilitate slower, sell imposed loads but and J. M Lawrence, eds. A. A. Balkema. Rotterdam.
MECHANICAL SPECIALIZATION OF PODIA 93
Fenner, D. H. 1973. The respiratory adaptations of the podia and am- Long, J. H. Jr., D. A. Pabst, W. R. Shepherd, and W. A. McLellan.
pullae ofechinoids (Echinodermata). Binl. Bull. 145: 323-339. 1997. Locomotor design ofdolphin vertebral columns: bending me-
Florey,E. A.,and M.A.Cahill. 1977. Ultrastructureofseaurchintube chanics and morphology of Delpluiui.t Jclphis. J. Ev/>. Binl. 2(10:
feet. Cell Tissue Res. 177: 195-214. 65-81.
Koehl, M. A. R. 1977. Mechanical diversity ofconnective tissue ofthe Wilkie.I.C.,R. H. Kmson,andC.M.Young. 1993. Smartcollagen in
body wall ofsea anemones. J. Exp. Biol. 69: 107-125. sea lilies. Nature 366: 519-520.
Long.J. H.Jr. 1992. Stiffness and damping forces in the intervertebral Wilson. J. A. and G. Hoyle. 1978. Serially homologous neurons as
jointsofblue marlin(Makairti nit'ricans'). J. E.\p. Biol. 162: 131-155. concomitants of functional specialisation. Nature 274: 377-378.