phoronida tamaño

7/27/2019 phoronida tamao

1/7

J . Zool., Lond. (1983) 200, 3 17-323

Size and shape in the phylum PhoronidaL A W R E N C E. A B E L E

Department of Biological Science, Florida State University, Tallahassee, Florida 32306,U.S.A .T O MG I L M O U R

Department ofBio logy, University qfsas katche wan , Saskatoon, SN7 0W0,CanadaA N D S A N D R A I L C H R I S T

Department of Biological Science, Florida State University, Tallahasse e, Florida 32306,U.S.A.(Accepted 12 October 1982)(With 2 figures in th e text)

The lophophorate phylum Phoronida consists of about 13 species, which differ in bodylength and width, number of longitudinal muscles, lophophore geometry and number oflophophore tentacles. In absolute terms large species have a larger body width, more ten-tacles, mor e longitudinal muscles and greater coiling of the lophophore than small species.However, size an d sha pe analyses suggest that with increasing size: ( I ) the body surface areato volume ratio increases because body length increases faster than body width; ( 2 ) th erelative number longitudinal muscles decreases, and ( 3 ) the relative feeding surface areaof the lophopho re decreases because tentacle diame ter is constant while tentacle num berincreases at the same rate as body length and tentacle length increases more slowly thantentacle numbe r. Coiling and spiraling of the lophop hore in large species may be an a ttemptto compensate for this last relationship. We suggest that the habits, mode of growth andfeeding mechanism of phoronids constrain size-related changes in shape.

PageontentsIntroduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31 7Methods and materials . . . . . . . . . . . . . . . . . . . . . . . . 31 8Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 319Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32 1References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32 3

IntroductionSize (measured by linear dimensions and mass) is often the single most important factorinfluencing morphology because of its geometric relationship to surface area and volume(Tho mp son, 1943). T he observed trend of increasing size within phylectic lines (Newell,1949), referred to as Copes Rule (Stanley, 1 973 ), is associated usually with allom etric aiter-

31 70022-5460/83/0303 1 7 + 0 7 803.00fO 0 983 Th e Zoological Society of London


2/7

318 L. G. ABELE E T A Lations in shape. A ny series of objects exhibiting isometry maintain s geometric similarity andundergoes a continuously decreasing ratio of surface area to volume with increasing size.In most phyla with a range of body sizes, larger animals offset isometric surface area tovolume relationships by changing shape, thereby partially compensating for mechanicalproblems such as those of locomotion or diffusion problems s uch as those of respiration andnutrition that would otherwise occur (Gould, 1966).

Despite the foundations established by Tho mp son (1943), Huxley (1932), Gould (1966),and Raup (1972), the influence of size on morphology rarely is addressed directly. Amonginvertebrates acoel turbellarians, archiannelid polychaetes, actinulid cnidarians, and thephoronid Phoronis ovufis often have been considered the most primitive representatives oftheir respective groups. Morph ological characteristics ar e traced from simplified systems inprimitive representitives to complex conditions common in more advanced taxa (e.g. thedigestive system of turbellarians or the lophophore of phoronids). In addition to beingconsidered primitive, the above groups all have relatively small body sizes. Thus, it maybe necessary to factor out quantitatively any size effect before assessing within-phylummorphological relationships. T h e importa nce of this consideration is illustrated by analysisof size and shape relationships within the phylum Phoronida.The phylum (also considered a class; Emig, 1977) Phoronida consists of two genera andapproximately 13 species (only 11 recognized by som e au thors; Em ig, 1979) of mostlyshallow-water, marine invertebrates, possessing lophophoral crowns. All are vermiform,tube-dwelling species, tending to be widely distributed in both temperate and tropicalregions. Preferred habitats of the species may by summarized by sediment type and depth.Generally, sm aller species are associated with hard substrates in the eulittoral an d sublittoralzones, while non-com men sal species are found in soft substrates of the eu littoral, sublittoral,and archib enthic zones (Emig, 1979). All forms are free-living, displaying a range of associ-ations from gregariousness to commensalism. Species range in length from 1.5 mm to450 mm , differing in body width, longitudinal muscle numbers, loph ophore geom etry, andtentacle numbers. Apparent morphological shifts within the phylum relative to the aboveparameters provide the major classificatory criteria for the species as well as the basis forconsideration of evolutionary trends within the phylum (Emig, 1971, 1976; Emig & Emig,1975).

Methods and materialsThe re is some question concerning the nu mb er of valid species in the phylu m Phoronid a. We haveused the classification of Emig ( 1 974 ) with the exception of Phoronis architecta, which was reared byT. Gilmour and will be considered a separate species from P. psammophi la. However, the additionor deletion of questionable species does not c hange our basic results. Th e data in T able I were derivedfrom Emig (19 74), Selys-Longchamp (1907), McIntosh ( 1 888), Cori (1890) and Stancyk et al. (1976)

except for P. architecta, which are based on NE. G ulf of Mexico specimens collected by T. Gilm our.Th ere is considerable disagreemen t regarding the co rrect statistical treatm ent for analysis of size andshape. Table 11 presents the results of least-squares regression and analysis. We used the standard powerfunction equ ation y = a 9 with the transformation to log J' = alog .x k log a. For linea r variables, a = 1indicates isometry, a > I positive allometry, an d a < 1 negative allo me try. Th e slopes were tested withStudent's t-test. The slope of the major axis of standardized variates (= reduced major axis = G Mregression) can be calculated simp ly by dividing the least-squares by the c orrel ation coefficient. Least-


3/7

SIZE AND SHAPE IN TH E P H Y L U M PHORONIDA 319TAB1.t IC'ompari l iw morphohg y of the Phoronidu

SpeciesNumber ofBody Body Num ber of Length of Diameter of longitudinallength (m m ) width (m m ) tentacles tentacles (rnm) tentacles (m m ) muscles

Phurunis hippocrep iuP. ovalisP. pallidaP. architectaP. psamm ophilaP. ijimaePhoronopsis harmeriPhoronis muelferiP. ausiralisP. husk iiP. hhaduriiPhoronopsis albomaculataPh. californica

1.5- 246- 1515-14022- 6925-16030-10040-22050-1 2050-20052- 6158- 9480-1 50

210-450

0.2-1 ' 50.25-0.350.3-1 '01.21-2.290.5-0.20 . 5 4 20.64 .00.2-1 .o2.0-5.02.01 .o0.5-2.0

2.5-5.0

16- 150I I - 285 0 - 14049- 9360- 13072- 21 6

100- 40040- 93600-1 00030-1000I406> I50070- 126

2-30.1-1 .2

2.50.8- 1.71.5- 2.52.0- 5.02.0- 5.01.0- 2.05.0-16.06.0- 7.06.5- 8.02.0- 3.02.0- 2. 5

0.0 50.052-0.05-0.070.060

0.0700-0270.052

--

24- 4314- 3918- 1934- 3925- 5337- 6979-13818- 3043- 87

-180-243

TABLE1Summary uf'.ptati.stic.s

Equation Significance AllometrictS , slope r F P s tatuslog anim al width = 0.51 1 log animal length - 0.920 0,236 0.547 4.685 0.050 Negativelog tentacle number = 0.929 log animal length $- 0 .555 0.325 0.653 8.196 0.017 Isometriclog tentacle length = 0.337 log anim al length - 0.178 0.224 0413 2.269 0.175 Not significantlog tentacle diameter = 0.0 7 log anim al length -- 1.318 0.133 0.069 0.024 0.884 Not significantlog tentacle length = 0.454 log tentacle numb er -- 0.586 0.105 0.792 18.606 0.002 Negativelog tentacle number=0.457 log animal length +0.837 0.190 0.647 5.768 0.030 Negativelog muscle number = 0.534 log animal length + 1.67 0.194 0.697 7.582 0.025 Negative

*Using the minimu m + maximum / 2 of measurements in Ta ble I; see Table I for n.?Slope tested against the isometric slope of " I ".squares , major axis , and the technique of Mos imann (1975 ) yield the same basic result. Individualphoronids ca n vary great ly in thei r length a nd width relat ionships , and therefore m inim um, m aximu m,and m in imum p lus maximum d ivided by two of the values in Table I were used i n the analyses. W ereport the latter results in Table I 1 and Figs I and 2, al though the u se of min imum and maximumgave sim ilar results.

ResultsThe following results are summarized in Figs 1 and 2 and Table 11. We realize the short-comings of the data but these are all that are available from the literature. Rather than


4/7

320( 0 )200 - .

II)i- loo= 00 -ur2 50-F

0- .0 0 .- -

L 8: 0 - ..I 1 1 1 1 1 1 1 1 I I I L

L. G. ABELE E T AL.

Body length (rnrn)

10 50 100 300 1000 04 0-3 0.50.7 1.0 2 4Tentacle number Body width (mm)

FIG. . (a) Plot of the relationship between number of longitudinal muscles and body length. (b) Body width plot-ted against body length. (c) Tentacle length plotted against tentacle num ber. (d) Number of longitudinal musclesplotted against body width. Note all plots are log-log and the equations for each relationship are given in Table11.

examine each equation in detail we would prefer simply to state the trends in size and shapefor the characters under consideration.Overall body diameter is negatively allometric relative to body length; as a result larger

species are relatively narrow compared with small species (Fig. l(b)). The ratio of bodysurface area to volume is therefore greater in largest than in smallest species. This resultsfrom the forced sensitivity (w


5/7

SIZE AND SHAPE IN T H E P HYLUM P HOR ONIDA 32 15000

2500

1000In2 50 00C++ 250z..-a5 100z

50

25

---------- I Y

U

101 ' I I I I I I 1 I10 25 50 100 250 500 1000Body l ength ( m m )

FIG. . A log-log plot ofthe relationship between body length and number oflophophore tentacles in the phylumPhoronida. The shapes of the lophophores are shown in cross-section along an approximate regression line. Thesymbols indicate the various species that have the same lophophore shape; only Phoronopsis californica (no. 6 inthe lower right) has double , conical helices (after Emig, 1974). Th e species are from left to right for each symbol:0 = Phoronis ovalis; A = P. muelleri; = P. hippocrepia; P . architecta, P. ijimai, P. pallida, P . psammophila,Phoronopsis albomaculata; A = P. harmeri; = P. buskii, P , bhadurii, P. australis; * = Phoronopsis californica.

DiscussionWe suggest that the habits, mode of growth an d feeding mechanism of phoron ids imposelimits on size-related changes in shape.There appear to be two constraints on the relationship between body length and width.The animal must be able to retract itself into the tube to avoid predation, and therefore,in order for longitudinal muscles to operate efficiently, the length of the animal must besubstantially greater than its width. S econd, the cross-sectional area at the distal end of theworm where the lophophore is located should be small so that the cilia on the tentacles cancreate a water current with a minimum of dead space. We infer this latter constraint fromthe limitation of osculum diam eter in asconoid sponges (Bidder, 1923; Reiswig, 1975). Th erelative increase in the ratio of body surface-area to v olum e may be related to the postulatedintake of dissolved nutrients across the body surface (Emig & Thouveny, 1976).As a consequence of the constraints on the body length : width relationships outlinedabove, the nu mber of longitudinal muscles may be limited by space. Longitudinal musclesoccur medially to a thin layer of circular muscle and appear as bundles that project exten-sively into the coelom toward the middle of the b ody (Hy ma n, 1959). Compensation forthe relative decrease in strength could occur by modification of muscle structure. Such apossibility is suggested by the zonation of muscu lature observed in Phoronis pullidu (cf. SilCn,


6/7

322 L. G. ABELE E T A L .1952). An other modification of structure th at m ay be related to a relative decrease in musclenum ber is the thickening and development of an an terior collar fold, a diagnostic character-istic of the genus Phoronopsis. Species in this genus are the largest in the phylum and thecollar fold may provide additional suppo rt for the large lophoph ore. O ther large species, suchas P. australis, may have adopted a lifestyle that does not req uire additional crown su ppo rt.There is a relative decrease in the feeding surface area of the lop hop hore in large species.The lophophore of the smallest species (P. ovalis) consists of a double row of tentaclesarranged in a circlet around the m outh. A s the num ber of tentacles increases in larger species,the ring assumes the shape of a double horseshoe. With further increase in tentacle num ber,the shape is of double spirals with 1.5 to 3.5 coils on each side. Th e loph opho re of the largestspecies, Phoronopsis californica, consists of double conical helices with four, five o r mo recoils on each side (Fig. 2). At the bottom of the space between the tentacles there is anepistome covering a pair of oral grooves extending from a central m outh .Feeding is by water currents generated by lateral cilia of adjacent tentacles (see Gilm our,1979). Th is feeding method apparently imposes several restraints on the increase of tentacu-lar surface area during growth since tentacle diameter is approximately the same in allspecies (Table I). A significant increase in the tentacle diameter could cause light, ediblematerial to be entrained by rejectory cilia. If intertentacular distances increased, the relativeproportion of filtered material could decrease. Decreasing distances between tentacles cou ldcause lateral cilia to collide and thus lose efficiency. Since waste materials are transportedupward to the tentacle tips for expulsion, a significant increase in tentacle length coulddecrease the effectiveness of the rejectory system and could cause reintroduction of heavy,inedible particles by incoming water currents. Thus, it follows that there are optimumdimensions for the length an d diam eter of the tentacles an d that surface area can be increasedwithout loss of efficiency only by addition of tentacles at a standard distance from oneanother.The spiraling pattern of the lophophore observed with size increases may represent amechanism to compensate for the relative decrease in feeding surface area imposed bytentacle length and diameter con straints. Tw o criteria considered for evaluating the successof biophysical changes are fulfilled by lophophore variations observed in phoronids. Thefirst is a thermod ynam ic requiremen t that the con dition ap pears in response to minimizationof energy. Th e second is a m echanical requiremen t tha t the cond ition mu st result from basicmaterials already available. A further consequence of the geom etric innovation of the spiral-ing pattern (seen also in some polychaetes) is to increase water propulsion efficiency bysequentically accelerating particles by cilia located at various levels of the spiral.During growth (after postlarval metamorphosis), additional tentacles are formed in themiddle of the inner two parallel tentacu lar rows. Full length of these new tentacles is attainedrapidly and the tentacles are shifted laterally as subsequent on es are formed (Hy ma n, 195 9).Consequently, lophophore growth is accompanied by continuously changing relationshipsamong the tentacles, the epistome, and the oral grooves that lie beneath the epistome. (Apossible exception to this relationship may be after lophophoral autonomy; Emig, 1972.)Th us there can be n o overt differentiation of specialization of tentacles for particle rejectionor acceptan ce as has occurred in som e brachiopods (G ilmo ur, 197 9). In view of our findingswith Phoron ida, the inferred size-required allometry in brach ipods (W estoll, 1950) mightdeserve reexamination since specialization of tentacles and cilia may compensate for size-related changes in feeding surface area of brachiopods.


7/7

SIZE AN D SHAPE IN T H E PH Y L UM PH O RO N ID A 323In summary, body plan, growth patterns, and feeding methods of phoronids limit size-related morphological changes. Phoronid morphology thus is influenced by a historicalphylogenetic factor (limits inherent in the body plan), a functional factor (metho d of feeding),and a structural factor (method of tentacle ad dition) (Seilacher, 1973).

W e t h a n k E. Connor. N . Gotel l i , S. Could. F. J a m e s , J . M o s i m a n n . D. Simber lo f f . D. St ro n g , an dC. Young for c o m m e n t s . A r l e e M o n t a l v o p r o v i d e d Figure I . T he Fl o r i d a S t a t e U n i v e r s i t y p ro v i d edc o m p u t i n g t i m e .

R E F E R E N C E SBidder, G. P. (1923 ). The relation of the form o f a sponge to its currents. Q. J I microsr. Soc. 67: 293-325.Cori, C. J. (1980). Untersuchungen iiber die Anatomie und Histologie der Gattung Phoronis . Z. win. Zool. 51 :Emig. C. C. (1971). Taxonom ie et systematique des Phoronidiens. Bull. M u s . nut. Hist. nu t . (3 )8: 469-568.Emig, C. C. (1972). Regeneration de la region anterieure de Phoronsis psammophila Cori (Phoronida). Z . Morph.Emig. C . C. (1974). Th e systematics and evolution o fth e phylum Phoronida. Z . zoo/.Syst. EvolForsch. 12: 128-1 5 1 .Emig. C. C. (1976). Le ophophore structure significative de Lophophorates (Brachiopodes, Bryozoaires, Phoroni-Emig, C. C. ( 1977). Notes sur la localisation, I'ecologie et la taxonomie des Phoronidiens. Tethys 7: 357-364.Emig, C. C. (1979). British and other phoronids. Synopses Br . Fauna No. 13.Emig, C. C. & Emig, A. ( I 975). Etude des variations du nombre et de la repartition des muscles longitudinauxEmig. C. C. & Thouv eny. Y. (1976). Absorption directe d'un acide am ine par Phoronis psamm ophila . Mar. Biol..Gilmour, T. ( 1 979). Ciliation and function of food-collecting and waste rejecting organs of lophophorates. Can.Gould, S. J . (1966 ). Allom etry and size in ontogeny and phylogeny. Biol. Rei'. 41: 5 8 7 6 4 0 .Huxley. J. S. (1932). Problems qf relative growlh. London: Methuen.Mclntosh. W. C. (1888). Report on Phoronis huskii n. sp.. dredged during the Voyage of HMS Challenger.Mosimann. J. E. (1975). Statistical distribution in scientjfic work 2. Dordrecht. Holland: D. Reidel Co.Newell, N. D. (1949). Phyletic size increase, an important trend illustrated by fossil invertebrates. Evrtltction.Raup. D. M. (1972). Approaches to morphologic analysis. In J1ollrl.r irr pa /echo log j8 :1845. Schopf, T. J . M.Reiswig, H. M. (1975 ). Th e aquiferous systems of thr ee Desmospongidae. J. hlorph. 145: 493-502.Seilacher, A. (19 73). Fabric ational noise in adaptiv e morphology. Sysr. Zool. 22: 451-465.Selys-Longchamps. M. De (1907). Phoronis. Fuuna Flora GolfNrapel. No. 30 .Silkn. L. (1952). Research o n P horonidea oft he G ullmar Fiord area (west coast ofSweden). 4rk. Zoo l . (2 ) 4: 95-140.Stancyk, S. E., Maturo. F. J . S. & Hea rd, R. W . (1976 ). Phoro nids from the east coast of the United States. Bull.Stanley. S. M. (1973) . An exp lanation for Cope's Rule. Evolution, h n c n s t e r . Pa. 27: 1-26.Thompson, D'Arcy W. ( 1 943). On growth and /brm . Cambridge: Cam bridge University Press.Westoll. T. S. (1950). Some aspects of growth studies in fossils. Proc. R . SOL-. and. (B) 137: 490-509.

480-568.

Tiere 73: 117-144.

diens). Zool. Scr. 5: 133-1 37.

chez Phoronis psammophila Cori. J . e x p . m a r. B i d . Ecol. 17: 23-3 1.Berl. 37: 69-73.J. Zoo/. 56: 2142-2155.

1873-1876. Rep. liry. H h S Challenger IZoo l . l27 : 1-27.

L u n c u w r . Pu. : 103-124.(Ed.). San Francisco: Freem an, Cooper and Co.

m u . ri . 26: 576-584.

phoronida tamaño

Documents

Transcript of phoronida tamaño