A system of cuticular nomenclature based on the strata observed in Enoplia is proposed. Nematode cuticle is divided into four fundamental strata: epicuticle, exocuticle, mesocuticle, and endocuticle. Application of this system allows the correlation of complementary strata throughout Nemata. The major taxonomic categories within Nemata are differentiated on the basis of their cuticular strata as compared with the Enoplia model cuticle

Maggenti, Armand R.

English

DigitalCommons@University of Nebraska

University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 1-1979 The Role of Cuticular Strata Nomenclature in the Systematics of Nemata Armand R. Maggenti University of California - Davis Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs  Part of the Parasitology Commons Maggenti, Armand R., "The Role of Cuticular Strata Nomenclature in the Systematics of Nemata" (1979). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 98. https://digitalcommons.unl.edu/parasitologyfacpubs/98 This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. The Role of Cuticular Strata Nomenclature in the Systematics of Nemata A. R. MAGGENTI  1 Abstract: A system of cuticular nomenclature based on the strata observed in Enoplia is proposed. Nematode cuticle is divided into four fundamental strata: epicuticle, exocuticle, mesocuticle, and endocuticle. Application of this system allows the correlation of complementary strata throughout Nemata. The major taxonomic ategories within Nemata are differentiated on the basis of their cuticular strata as compared with the Enoplia model cuticle. Key Words: cuticle, Enoplia. classification. Systematists have long utilized external modifications and specialized organs of the cuticle to separate species, genera, families, etc. Even today, with our improved knowl- edge of internal structures and organs, the external cuticle remains a basic character to the taxonomist. Perhaps the importance given cuticle in taxonomy is justified by the fact that tile hypodermis is a remnant of embryological ectoderm, retaining tile prim- itive potential of the tissue. That  potential is shown in diverse integumental organs functioning in secretion, excretion, and sen- sation. Furthermore, the glands of the body and the cuticle of body invaginations are appreciated more fully if they are recog- nized as derivitives of ectoderm. Since the external modifications and manifestations of the cuticle have played a major role in our systematic oncepts, it seems plausible that the internal structuring of nema integument could be useful in examination of current systematic concepts. Nematode cuticle is commonly de- scribed as a laminated noncellular elastic secretion of the hypodermis. Although numerous studies have been conducted with light microscopy, TEM, and SEM, we continue to have little understanding of this complex organ that interfaces the nema with its external environment. Studies of ascarid cuticle with the Iight microscope and TEM (3, 6, 10, 22) serve as the basis for contemporary interpreta- tions of nematode cuticle. Ti le model ascarid cuticle has nine layers distributed among three strata designated as tile cortical, matrix (median), and basal layers. It has been assumed that these same strata occur in all Nemata and the terms have been used in a manner that implies they Received for publication 8 June 1978. 1 Nematologist. Division of Nematology, University of Cali- fornia, Davis 95616. 94 have chemical or functional relationships that prove them homologous within Nemata. In fact, such relationships have not been proved, and superimposition of this terminology throughout is misleading. Bird (3) pointed out that "the diversity in Nomenclature of the various layers of the nematode cuticle has resulted in some con- fusion." After a review of cuticular studies I believe that the laminated strata and their sequential order can bave significance and correlation throughout Nemata if an enoplid cuticle model is used. There is little purpose in attempting any under- standing of cuticular strata following current nomenclature. One simply cannot talk about or see an orderly sequence among Nemata for the "so-called" median (homogeneous matrix) layer or the basal layer. Recent reviews attempting to do that have broken down because current concepts based on Ascaris do not allow for compari- son, primarily because of the assumption that all nema cuticles have the complete complement of cortical, median, and basal layers (3, 4). It is my premise that continu- ing to view cuticle on that basis will impede correlation of cuticular characteristics with our understanding of nematode systematics. Furthermore, Hinz (9) finds no justification for designating the cortical, fibril, and homogeneous (= median) layers in Para- scaris equorum as separate strata, and he treats them as substrata of the cortical ayer. A topographic system of nomenclature utilizing an enoplid for reference is pre- sented here. Of the nematodes tudied, Denontostoma of Enoplia offers the most complete sequence of cuticular strata. The  toponyms are all based on the noun 'cuticle' modified by adjectives connoting relative positions and, as such, the integument is divided into four fundamental strata: J Nematol. 1979 January; 11(1): 94–98. epicuticle, exocuticle, mesocuticle, and endocuticle. Fig. 1 applies the toponyms to the rec- ognized strata in Deontostoma (21). This concept correlates cuticular strata through- out Nemata with an Enoplia model and allows for the absence of certain strata depending upon the cuticle under consid- eration. For example, in the cuticle of Ascaris only three strata are recognized: epicuticle, exocuticle and mesocuticle; current studies show no evidence of endo- cuticle. Applying this system, based on Enoplia, to the Nemata we can recognize differences between Adenophorean and Secernentean cuticle. We can further differentiate, on the basis of the nature of tile strata, Enoplia from Chromadoria. In Secernentea it is possible to distinguish among Rhabditida, Spirurida, Strongylida, and Tylenchida. Therefore, our major taxonomic divisions aml phylogenetic oncept are confirmable by this system. That  cannot be done with systems based on cortical, median, and basal layers. For instance, tile "basal" layer of Ascaris (22) is not the same stratum as the "basal" layer of Meloidogyne (2) or the "basal" layer of Xiphinema (19). In fact, those are different strata in each of the genera named. In the system proposed here, the "basal" layers of those genera are rec- ognized as exocuticle in Meloidogyne, mesocuticle in Ascaris, and endocuticle in Xiphinema. Fig. l, utilizing diagrams based on TEM studies, illustrates the application of this concept and its conformity to our current taxonomic concepts. To  show strata iden- tifications the diagrams are scaled, where feasible, to Enoplia; the thicknesses of strata do not represent actual measure- ments. For purpose of simplification the cuticles diagrammed are based on main body cuticle studies; anterior and caudal cuticles are excluded. The characteristics of the four funda- mental strata derived from an enoploid model are as follows: Epicuticle: The outermost stratum, typically tri-laminate and consisting of two electron-dense layers separated by an electron-transparent zone. In at least two nematodes, Meloidogyne iavanica and Tri- chinella spiralis (4), the outer electron-dense Cuticular Strata Nomenclature: Maggenti 95 layer appears also to be triple-layered. Exocuticle: This stratum is subdivisible into two or more sublayers. In Enoplida it contains two substrata: an outer lamina- tion composed of a finely granular dense substance. The inner substratum, common to much of Nemata, consists of fine radially oriented striae, which at higher resolu- tion appear to be formed from two electron-dense plates separated by an electron-transparent core. Body wall canals may extend through the exocuticle. Mesocuticle: This stratum is composed of organized rods, fibers, plates, or struts. In the enoplid model this stratum consists of fibrous layers arranged obliquely at 45 to 55 ° from each other. The  number of sub- strata is variable. Endocuticle: The substrate of this layer is poorly defined. The substratum often appears to be penetrated by hypodermal extensions and muscle attachment. In TEM photos and reconstructions of the endo- cuticle it sometimes appears to have a feathery fibroidal consistency. Among Enoplia the presence of all strata is remarkably constant. The mesocuticle varies by the number of fiber layers, their direction, and angular relationship. The  evolutionary trend (Fig. l) seems to be reflected in a reduction of the number of substrata and oblique fibers (I, 8, 11, 15, 17, 18, 19, 21). The thickness of endocuticle is also variable, showing strong develop- ment in tile insect parasite Mermis (15). The structure of the cuticle of Trichodorus (18) has been poorly resolved and currently has as a distinct stratum only the epicuticle. Chromadoria are distinguished by the striking modifications of the mesocuticle (16, 23, 24), which may be platelike or a combination of oblique fibers and a "fluid" substratum with structural struts. Tile similarity in cuticular structure of dcanthonchus (24), Chrornadorina (16), and Caenorhabditis (7, 25) lends circum- stantial evidence to the hypothesis that Secernentea rose from chromadorid-like ancestors. The  literature indicates that the endocuticle occurs only in Rhabdit ida (7, 25). Filarids, Ascarida, Spirurida, and Strongylida are characterized by the pres- ence of only three strata: epicuticle, exocuticle, and mesocuticle (10, 12, 14, 22). In the larvae and adults of Cephalobidae 96 Journal of Nematology, Volume 11, No. 1, January 1979 [)COl+ t o',l a)11~ ,i .~l)~+ r t'e I ~t i nl +,'I Itl +s ADENOPHOREA Enop l ia  l , .ng  i d o ,'u • X i ph  i ne n la  NN :!:i ::~::: i~:i !:~ + Chromador ia  ]-~u c h r~Hu ado  ia  ep ieut lc le  ~ ~  ~ c 'xocul lc le  -~  : mesocu l i c le  endocut ic le -~. . . . . '~ . .~  ~ . . . . . . . . . . .  : : I . . . . .  I SECERNENTEA Mcrmi~ , ,~] -, ~ l r i chod  or . s  . . . .  ::~ ::i:Yi~ ¢~ l) i .  c it, phi, ma ,I i (;a e, no rhah dit i,, k,.cal is N il)p.,,t =-o ng ~, lu s / / . . . . .  adu l t  Pa . ac r  c l  lu ~ T-, I,:nc h ida  (20) and Ty lench ida  (2, 3, 4, 5, 13) and larval  Rhabd i t ida  (7, 25) and Strongyl ida (12, 14) ti le cuticle is l imi ted to two strata: epicut ic le and exocuticle. I t  also appears that  when the endo- cuticle and mesocutic le are present the ent i re cuticle is sited wi thout  layer resorp- tion. That  observat ion should be careful ly checked for endocut ic le  resorpt ion,  how- ever. It seems that the endocutic le,  mesocutic le or both act as a barr ier  to the mol t ing  fluids. In Ty lench ida ,  which lack these strata, the exocutic le is dissolved and "resorbed" with only the epicut ic le be ing shed (3). When all layers are present, as in chromador ids ,  the ent i re cuticle is repor ted  to shed (3). Taxonomica l ly ,  an area of par t icu lar  interest is the ambigu i ty  of the p lacement  o~ Dioctoph),ma renale. Its taxonomic  char- acters are in some measure inconsistent with its p lacement  in Adenophorea  near  Dory- la imida or Mermis. Characters such as a male reproduct ive  system with single testis, spicule e longate and single, and a bursa l ike extension around male cloaca (= "sucker") are associated more typical ly with Secern- entea rather  than wi th  Adenophorea  (17). In Fig. l the schematic i l lustrat ion would  also support  a Secernentean re lat ionship,  No endocut ic le  is evident;  in fact, the cnticle is very s imi lar  to that of Ascaris. It is thus apparent  hat this nematode requires closer study. At any rate, the current  hy- pothesis tends to confirm the ambigu i ty  of the p lacement  of Dioctophyma as an Adenophorean .  Cons iderat ion of cuticle in this l ight indicates that there is a re lat ionsh ip  of cut icular  strata among nematodes.  The  hypothesis presented here al lows for mean- ingful  compar ison of nematode cuticles. T i le  t rad i t iona l  app l i cat ion  of s imi lar  names to diss imi lar  strata h inders  our  unders tand ing  of strata and their  chemistry and function. More at tent ion  needs to be Cut icu lar  Strata Nomenc la ture :  Maggenti 97 directed to interna l  cuticle as well  as to the secondary depos i t ion  of " inf racut ic le"  seen in the anter ior  of such widely d ivergent  groups as Dory la imida  and Ty lench ida.  Studies indicate that the nature  of anter ior  and caudal  cuticle may well  be highly sig- nificant. Grootaer t  and L ippens  (8) po int  out  that in Dory la imida  anter ior  infra- cuticle appears to be a secondary fo rmat ion  which may be va luable  in eva luat ing the categories of Dory la imida.  Such a view is complementary  to the system presented here and clearly indicates why we should d iscard the old nomenc lature  which does not have the f lexibi l i ty to incorporate  or ut i l ize valu- able observat ions such as those suggested by Grootaer t  and L ippens.  L ITERATURE C ITED 1. ABOUL-EID, H. Z. 1969. Electron microscope studies on the body wall and feeding apparatus of Longidorus macrosoma. Nema- tologica 15:451-463. 2. BIRD, A. F. 1968. Changes associated with parasitism in nematodes. III. Ultrastructure of the egg shell, Larval cuticle, and contents of the subventral esophageal glands in Meloidogyne javanica, with some observations on hatching. J. Parasitol. 54:475-489. 3. BIRD, A. F. I971. The structure of nematodes. Academic Press, New York and London. 318 pp. 4. BIRD, A. F. 1976. The development and organi- zation of skeletal structures in nematodes. Pages 11)7-137 in: The Organization of Nema- todes. N. A. Croll, ed., Academic Press, London, New York, San Francisco. 5. BYERS, J. R., and R. V. ANDERSON. 1972. Ultrastructural morphology of the body wail, stoma, and stomatostyle of the nematode, Tylenchorhynchus dubius (Buetscli, 1873) Filipjev. 1936. Can. J. Zool. 50:457-465. 6. CHITWOOD, B, G., and M. B. CHITWOOD. 1950. An introduction to nematology. Sect. 1: Anatomy, Rev. Ed., Monumental Press, Balti- more, Maryland. 213 pp. 7. EPSTEIN, J., J. CASTILLO, S. HIMMEL- HOCH, and B. M. ZUCKERMAN. 1971, Ultrastructural studies on Caenorhabditis briggsae. J Nematol. 3:69-78. 8. GROOTAERT, P., and P. L. LIPPENS. 1974. • ~ I l t l l  \ \ \ \ \  FIG. I. Schematic representation of nematode cuticles and strata relationships to a Deontostoma model. Mesocuticle comparisons are shown by shaded connections. Deontostoma, based on TEM, Siddiqui and Viglierchio, 1977; Aporcelaimellus, based on Grootaert and Lippens, 1974; Longidorus, based on Aboul-Eid, 1969; Xiphinema, based on Roggen et al., 1967; Mermis and Dioctophyma based on Chitwood and Chitwood, 1950; Trichodorus based on TEM, Raski et al., 1969; Euchromadora, based on Watson, 1965; Acanthonchus, based on ~Vright and Hope, 1968; Caenorhabditis, based on Zuckerman et al., 1973; Asearis, based on TEM, Watson, 1965; Nippostrongylus, based on TEM, Jamuar, 1966; Panagrellus, based on TEM, Samoiloff, 1973. J 98 Journal of Nematology, Volume 11, No. 1, January 1979 Some ultrastructural changes in cuticle and hypodermis of Aporcelaimellus during the first molt (Nematoda: Dorylaimoidea). Z. Morph. Tiere 79:269-282. 9. HINZ, E. 1963. Electronenmikroskopische untersuchungen an Parascaris equorum (integument, isolationgewebe, muskulatur und nerven). Protoplasma 56:202-241. 10. INGLIS, W. G. 1964. The comparative anatomy of the ascaridoid cuticle (Nematoda). Bull. Soc. Zool. France 89:317-338. 11. INGLIS, W. G. 1964. The structure of the nematode cuticle. Proc. Zool. Soc. Lond. 143: 465 -502. 12. JAMUAR, M. P. 1966. Electron microscope studies on the body wall of the nematode Nippostrongylus brasiliensis. J Parasitol. 52: 209-232. 13. KISIEL, M. S.. S. HIMMELHOCH, and B. M. ZUCKERMAN. 1972. Fine structure of the body wall and vulva area of Pratylenchus penetrans. Nematologica 18:234-238. 14. LEE, D. L. 1965. An electron microscope study of the body wall of the third-stage larva of Nippostrongylus brasiliensis. Parasitol. 56: 127-135. 15. LEE, D. L. 1970. The ultrastructure of the cuticle of adult female Mermis nigrescens (Nematoda). J Zool. Lond. 161:513-518. 16. LIPPENS, P. L. 1974. Ultrastructure of a marine nematode, Chromadorina germanica (Buetschli, 1874). II. Cytology of lateral epidermal glands and associated neurocytes. Z. Morph. Tiere 79:283-294. 17. LIPPENS, P. L., A. COOMANS, A. T. DeGRISSE, and A. LAGASSE. 1974. Ultra- structure of the anterior body region in Aporcellaimellns obtusicaudatus and A. ob- scurus. Nematologica 20:242-256. 18. RASKI, D. J., N. O. JONES, and D. R. ROGGEN. 1969. On the morphology and ultrastruciure of the esophageal region of Trichodorus allius Jensen. Proc. Hehninthol. Soc. Wash. 36:106-118. 19. ROGGEN, D. R., D. J. RASKI, and N. O. JONES. 1967. Further electron microscopic observations of Xiphinema index. Nema- tologica 13:1-16. 20. SAMOILOFF, M. R. 1973. Nematode morpho- genesis: pattern of transfer of protein to the cuticle of adult Panagrellus silusiae (Cephalobidae). Nematologica 19:15-18. 21. SIDD1QUI, I., and D. R. VIGLIERCHIO. 1977. Ullrastructure of the anterior body region of marine nematode Deontostoma californicnm. J. Nematol. 9:56-82. 22. WATSON, B. D. 1965. The fine structure of the body-wall and the growth of the cuticle in the adult nematode Ascaris lumbricoides. Quart. J. Micr. Sci. 106:83-91. 23. WATSON. B. D. 1965. The fine structure of the body-wall in a free-living nematode, Euchromadora vulgaris. Quart. J. Micr. Sci. 106:75-81. 24. WRIGHT, K. A., and W. D. HOPE. 1968. Elaborations of the cuticle of Acanthonchus duplicatus Wieser, 1959 (Nematoda: Cy- atholaimidac) as revealed by light and electron microscopy. Can. J. Zool. 46:1005- 1011. 25. ZUCKERMAN, B. M., S. HIMMELHOCH, and M. KISIEL. 1973. Fine structure changes in the cuticle of adult Caenorhabditis briggsae with age. Nematologica 19:109-112. 

The Role of Cuticular Strata Nomenclature in the Systematics of Nemata

UNL | Libraries

University of Nebraska - Lincoln 
DigitalCommons@University of Nebraska - Lincoln 
Faculty Publications from the Harold W. Manter 
Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 
1-1979 
The Role of Cuticular Strata Nomenclature in the Systematics of 
Nemata 
Armand R. Maggenti 
University of California - Davis 
Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs 
 Part of the Parasitology Commons 
Maggenti, Armand R., "The Role of Cuticular Strata Nomenclature in the Systematics of Nemata" (1979). 
Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 98. 
https://digitalcommons.unl.edu/parasitologyfacpubs/98 
This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at 
DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from 
the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of 
Nebraska - Lincoln. 
The Role of Cuticular Strata Nomenclature 
in the Systematics of Nemata 
A. R. MAGGENTI  1 
Abstract: A system of cuticular nomenclature based on the strata observed in Enoplia is proposed. 
Nematode cuticle is divided into four fundamental strata: epicuticle, exocuticle, mesocuticle, and 
endocuticle. Application of this system allows the correlation of complementary strata throughout 
Nemata. The major taxonomic ategories within Nemata are differentiated on the basis of their 
cuticular strata as compared with the Enoplia model cuticle. Key Words: cuticle, Enoplia. 
classification. 
Systematists have long utilized external 
modifications and specialized organs of the 
cuticle to separate species, genera, families, 
etc. Even today, with our improved knowl- 
edge of internal structures and organs, the 
external cuticle remains a basic character 
to the taxonomist. Perhaps the importance 
given cuticle in taxonomy is justified by the 
fact that tile hypodermis is a remnant of 
embryological ectoderm, retaining tile prim- 
itive potential of the tissue. That  potential 
is shown in diverse integumental organs 
functioning in secretion, excretion, and sen- 
sation. Furthermore, the glands of the body 
and the cuticle of body invaginations are 
appreciated more fully if they are recog- 
nized as derivitives of ectoderm. 
Since the external modifications and 
manifestations of the cuticle have played a 
major role in our systematic oncepts, it 
seems plausible that the internal structuring 
of nema integument could be useful in 
examination of current systematic concepts. 
Nematode cuticle is commonly de- 
scribed as a laminated noncellular elastic 
secretion of the hypodermis. Although 
numerous studies have been conducted 
with light microscopy, TEM, and SEM, we 
continue to have little understanding of 
this complex organ that interfaces the nema 
with its external environment. 
Studies of ascarid cuticle with the Iight 
microscope and TEM (3, 6, 10, 22) serve 
as the basis for contemporary interpreta- 
tions of nematode cuticle. Ti le model 
ascarid cuticle has nine layers distributed 
among three strata designated as tile 
cortical, matrix (median), and basal layers. 
It has been assumed that these same strata 
occur in all Nemata and the terms have 
been used in a manner that implies they 
Received for publication 8 June 1978. 
1 Nematologist. Division of Nematology, University of Cali- 
fornia, Davis 95616. 
94 
have chemical or functional relationships 
that prove them homologous within 
Nemata. In fact, such relationships have 
not been proved, and superimposition of 
this terminology throughout is misleading. 
Bird (3) pointed out that "the diversity in 
Nomenclature of the various layers of the 
nematode cuticle has resulted in some con- 
fusion." 
After a review of cuticular studies I 
believe that the laminated strata and their 
sequential order can bave significance and 
correlation throughout Nemata if an 
enoplid cuticle model is used. There is 
little purpose in attempting any under- 
standing of cuticular strata following 
current nomenclature. One simply cannot 
talk about or see an orderly sequence 
among Nemata for the "so-called" median 
(homogeneous matrix) layer or the basal 
layer. Recent reviews attempting to do that 
have broken down because current concepts 
based on Ascaris do not allow for compari- 
son, primarily because of the assumption 
that all nema cuticles have the complete 
complement of cortical, median, and basal 
layers (3, 4). It is my premise that continu- 
ing to view cuticle on that basis will impede 
correlation of cuticular characteristics with 
our understanding of nematode systematics. 
Furthermore, Hinz (9) finds no justification 
for designating the cortical, fibril, and 
homogeneous (= median) layers in Para- 
scaris equorum as separate strata, and he 
treats them as substrata of the cortical ayer. 
A topographic system of nomenclature 
utilizing an enoplid for reference is pre- 
sented here. Of the nematodes tudied, 
Denontostoma of Enoplia offers the most 
complete sequence of cuticular strata. The  
toponyms are all based on the noun 'cuticle' 
modified by adjectives connoting relative 
positions and, as such, the integument is 
divided into four fundamental strata: 
J Nematol. 1979 January; 11(1): 94–98. 
epicuticle, exocuticle, mesocuticle, and 
endocuticle. 
Fig. 1 applies the toponyms to the rec- 
ognized strata in Deontostoma (21). This 
concept correlates cuticular strata through- 
out Nemata with an Enoplia model and 
allows for the absence of certain strata 
depending upon the cuticle under consid- 
eration. For example, in the cuticle of 
Ascaris only three strata are recognized: 
epicuticle, exocuticle and mesocuticle; 
current studies show no evidence of endo- 
cuticle. 
Applying this system, based on Enoplia, 
to the Nemata we can recognize differences 
between Adenophorean and Secernentean 
cuticle. We can further differentiate, on the 
basis of the nature of tile strata, Enoplia 
from Chromadoria. In Secernentea it is 
possible to distinguish among Rhabditida, 
Spirurida, Strongylida, and Tylenchida. 
Therefore, our major taxonomic divisions 
aml phylogenetic oncept are confirmable 
by this system. That  cannot be done with 
systems based on cortical, median, and basal 
layers. For instance, tile "basal" layer of 
Ascaris (22) is not the same stratum as the 
"basal" layer of Meloidogyne (2) or the 
"basal" layer of Xiphinema (19). In fact, 
those are different strata in each of the 
genera named. In the system proposed here, 
the "basal" layers of those genera are rec- 
ognized as exocuticle in Meloidogyne, 
mesocuticle in Ascaris, and endocuticle in 
Xiphinema. 
Fig. l, utilizing diagrams based on TEM 
studies, illustrates the application of this 
concept and its conformity to our current 
taxonomic concepts. To  show strata iden- 
tifications the diagrams are scaled, where 
feasible, to Enoplia; the thicknesses of 
strata do not represent actual measure- 
ments. For purpose of simplification the 
cuticles diagrammed are based on main 
body cuticle studies; anterior and caudal 
cuticles are excluded. 
The characteristics of the four funda- 
mental strata derived from an enoploid 
model are as follows: 
Epicuticle: The outermost stratum, 
typically tri-laminate and consisting of two 
electron-dense layers separated by an 
electron-transparent zone. In at least two 
nematodes, Meloidogyne iavanica and Tri- 
chinella spiralis (4), the outer electron-dense 
Cuticular Strata Nomenclature: Maggenti 95 
layer appears also to be triple-layered. 
Exocuticle: This stratum is subdivisible 
into two or more sublayers. In Enoplida it 
contains two substrata: an outer lamina- 
tion composed of a finely granular dense 
substance. The inner substratum, common 
to much of Nemata, consists of fine radially 
oriented striae, which at higher resolu- 
tion appear to be formed from two 
electron-dense plates separated by an 
electron-transparent core. Body wall canals 
may extend through the exocuticle. 
Mesocuticle: This stratum is composed 
of organized rods, fibers, plates, or struts. 
In the enoplid model this stratum consists 
of fibrous layers arranged obliquely at 45 to 
55 ° from each other. The  number of sub- 
strata is variable. 
Endocuticle: The substrate of this layer 
is poorly defined. The substratum often 
appears to be penetrated by hypodermal 
extensions and muscle attachment. In TEM 
photos and reconstructions of the endo- 
cuticle it sometimes appears to have a 
feathery fibroidal consistency. 
Among Enoplia the presence of all strata 
is remarkably constant. The mesocuticle 
varies by the number of fiber layers, their 
direction, and angular relationship. The  
evolutionary trend (Fig. l) seems to be 
reflected in a reduction of the number of 
substrata and oblique fibers (I, 8, 11, 15, 
17, 18, 19, 21). The thickness of endocuticle 
is also variable, showing strong develop- 
ment in tile insect parasite Mermis (15). 
The structure of the cuticle of Trichodorus 
(18) has been poorly resolved and currently 
has as a distinct stratum only the epicuticle. 
Chromadoria are distinguished by the 
striking modifications of the mesocuticle 
(16, 23, 24), which may be platelike or a 
combination of oblique fibers and a "fluid" 
substratum with structural struts. 
Tile similarity in cuticular structure of 
dcanthonchus (24), Chrornadorina (16), 
and Caenorhabditis (7, 25) lends circum- 
stantial evidence to the hypothesis that 
Secernentea rose from chromadorid-like 
ancestors. The  literature indicates that the 
endocuticle occurs only in Rhabdit ida (7, 
25). Filarids, Ascarida, Spirurida, and 
Strongylida are characterized by the pres- 
ence of only three strata: epicuticle, 
exocuticle, and mesocuticle (10, 12, 14, 22). 
In the larvae and adults of Cephalobidae 
96 Journal of Nematology, Volume 11, No. 1, January 1979 
[)COl+ t o',l a)11~ ,i .~l)~+ r t'e I ~t i nl +,'I Itl +s 
ADENOPHOREA 
Enop l ia  
l , .ng  i d o ,'u • X i ph  i ne n la  
NN 
:!:i ::~::: i~:i !:~ + 
Chromador ia  
]-~u c h r~Hu ado  ia  
ep ieut lc le  ~ ~  ~ 
c 'xocul lc le  -~  : 
mesocu l i c le  
endocut ic le -~. . . . . '~ . .~  ~ . . . . . . . . . . .  : : I . . . . .  I 
SECERNENTEA 
Mcrmi~ 
, ,~] -, ~ 
l r i chod  or . s  
. . . .  ::~ ::i:Yi~ ¢~ 
l) i .  c it, phi, ma 
,I 
i 
(;a e, no rhah dit i,, k,.cal is N il)p.,,t =-o ng ~, lu s 
/ 
/ . . . . .  
adu l t  
Pa . ac r  c l  lu ~ T-, I,:nc h ida  
(20) and Ty lench ida  (2, 3, 4, 5, 13) and 
larval  Rhabd i t ida  (7, 25) and Strongyl ida 
(12, 14) ti le cuticle is l imi ted to two strata: 
epicut ic le and exocuticle. 
I t  also appears that  when the endo- 
cuticle and mesocutic le are present the 
ent i re cuticle is sited wi thout  layer resorp- 
tion. That  observat ion should be careful ly 
checked for endocut ic le  resorpt ion,  how- 
ever. It seems that the endocutic le,  
mesocutic le or both act as a barr ier  to the 
mol t ing  fluids. In Ty lench ida ,  which lack 
these strata, the exocutic le is dissolved and 
"resorbed" with only the epicut ic le be ing 
shed (3). When all layers are present, as in 
chromador ids ,  the ent i re cuticle is repor ted  
to shed (3). 
Taxonomica l ly ,  an area of par t icu lar  
interest is the ambigu i ty  of the p lacement  o~ 
Dioctoph),ma renale. Its taxonomic  char- 
acters are in some measure inconsistent with 
its p lacement  in Adenophorea  near  Dory- 
la imida or Mermis. Characters such as a 
male reproduct ive  system with single testis, 
spicule e longate and single, and a bursa l ike 
extension around male cloaca (= "sucker") 
are associated more typical ly with Secern- 
entea rather  than wi th  Adenophorea  (17). 
In Fig. l the schematic i l lustrat ion would  
also support  a Secernentean re lat ionship,  
No endocut ic le  is evident;  in fact, the 
cnticle is very s imi lar  to that of Ascaris. It 
is thus apparent  hat this nematode requires 
closer study. At any rate, the current  hy- 
pothesis tends to confirm the ambigu i ty  of 
the p lacement  of Dioctophyma as an 
Adenophorean .  
Cons iderat ion of cuticle in this l ight 
indicates that there is a re lat ionsh ip  of 
cut icular  strata among nematodes.  The  
hypothesis presented here al lows for mean- 
ingful  compar ison of nematode cuticles. 
T i le  t rad i t iona l  app l i cat ion  of s imi lar  
names to diss imi lar  strata h inders  our  
unders tand ing  of strata and their  chemistry 
and function. More at tent ion  needs to be 
Cut icu lar  Strata Nomenc la ture :  Maggenti 97 
directed to interna l  cuticle as well  as to 
the secondary depos i t ion  of " inf racut ic le"  
seen in the anter ior  of such widely d ivergent  
groups as Dory la imida  and Ty lench ida.  
Studies indicate that the nature  of anter ior  
and caudal  cuticle may well  be highly sig- 
nificant. Grootaer t  and L ippens  (8) po int  
out  that in Dory la imida  anter ior  infra- 
cuticle appears to be a secondary fo rmat ion  
which may be va luable  in eva luat ing the 
categories of Dory la imida.  Such a view is 
complementary  to the system presented here 
and clearly indicates why we should d iscard 
the old nomenc lature  which does not have 
the f lexibi l i ty to incorporate  or ut i l ize valu- 
able observat ions such as those suggested by 
Grootaer t  and L ippens.  
L ITERATURE C ITED 
1. ABOUL-EID, H. Z. 1969. Electron microscope 
studies on the body wall and feeding 
apparatus of Longidorus macrosoma. Nema- 
tologica 15:451-463. 
2. BIRD, A. F. 1968. Changes associated with 
parasitism in nematodes. III. Ultrastructure 
of the egg shell, Larval cuticle, and contents 
of the subventral esophageal glands in 
Meloidogyne javanica, with some observations 
on hatching. J. Parasitol. 54:475-489. 
3. BIRD, A. F. I971. The structure of nematodes. 
Academic Press, New York and London. 
318 pp. 
4. BIRD, A. F. 1976. The development and organi- 
zation of skeletal structures in nematodes. 
Pages 11)7-137 in: The Organization of Nema- 
todes. N. A. Croll, ed., Academic Press, 
London, New York, San Francisco. 
5. BYERS, J. R., and R. V. ANDERSON. 1972. 
Ultrastructural morphology of the body wail, 
stoma, and stomatostyle of the nematode, 
Tylenchorhynchus dubius (Buetscli, 1873) 
Filipjev. 1936. Can. J. Zool. 50:457-465. 
6. CHITWOOD, B, G., and M. B. CHITWOOD. 
1950. An introduction to nematology. Sect. 1: 
Anatomy, Rev. Ed., Monumental Press, Balti- 
more, Maryland. 213 pp. 
7. EPSTEIN, J., J. CASTILLO, S. HIMMEL- 
HOCH, and B. M. ZUCKERMAN. 1971, 
Ultrastructural studies on Caenorhabditis 
briggsae. J Nematol. 3:69-78. 
8. GROOTAERT, P., and P. L. LIPPENS. 1974. 
• ~ I l t l l  
\ \ \ \ \  
FIG. I. Schematic representation of nematode cuticles and strata relationships to a Deontostoma model. 
Mesocuticle comparisons are shown by shaded connections. Deontostoma, based on TEM, Siddiqui and 
Viglierchio, 1977; Aporcelaimellus, based on Grootaert and Lippens, 1974; Longidorus, based on Aboul-Eid, 
1969; Xiphinema, based on Roggen et al., 1967; Mermis and Dioctophyma based on Chitwood and Chitwood, 
1950; Trichodorus based on TEM, Raski et al., 1969; Euchromadora, based on Watson, 1965; 
Acanthonchus, based on ~Vright and Hope, 1968; Caenorhabditis, based on Zuckerman et al., 1973; Asearis, 
based on TEM, Watson, 1965; Nippostrongylus, based on TEM, Jamuar, 1966; Panagrellus, based on TEM, 
Samoiloff, 1973. 
J 
98 Journal of Nematology, Volume 11, No. 1, January 1979 
Some ultrastructural changes in cuticle and 
hypodermis of Aporcelaimellus during the 
first molt (Nematoda: Dorylaimoidea). 
Z. Morph. Tiere 79:269-282. 
9. HINZ, E. 1963. Electronenmikroskopische 
untersuchungen an Parascaris equorum 
(integument, isolationgewebe, muskulatur und 
nerven). Protoplasma 56:202-241. 
10. INGLIS, W. G. 1964. The comparative anatomy 
of the ascaridoid cuticle (Nematoda). Bull. 
Soc. Zool. France 89:317-338. 
11. INGLIS, W. G. 1964. The structure of the 
nematode cuticle. Proc. Zool. Soc. Lond. 143: 
465 -502. 
12. JAMUAR, M. P. 1966. Electron microscope 
studies on the body wall of the nematode 
Nippostrongylus brasiliensis. J Parasitol. 52: 
209-232. 
13. KISIEL, M. S.. S. HIMMELHOCH, and B. M. 
ZUCKERMAN. 1972. Fine structure of the 
body wall and vulva area of Pratylenchus 
penetrans. Nematologica 18:234-238. 
14. LEE, D. L. 1965. An electron microscope study 
of the body wall of the third-stage larva of 
Nippostrongylus brasiliensis. Parasitol. 56: 
127-135. 
15. LEE, D. L. 1970. The ultrastructure of the 
cuticle of adult female Mermis nigrescens 
(Nematoda). J Zool. Lond. 161:513-518. 
16. LIPPENS, P. L. 1974. Ultrastructure of a 
marine nematode, Chromadorina germanica 
(Buetschli, 1874). II. Cytology of lateral 
epidermal glands and associated neurocytes. 
Z. Morph. Tiere 79:283-294. 
17. LIPPENS, P. L., A. COOMANS, A. T. 
DeGRISSE, and A. LAGASSE. 1974. Ultra- 
structure of the anterior body region in 
Aporcellaimellns obtusicaudatus and A. ob- 
scurus. Nematologica 20:242-256. 
18. RASKI, D. J., N. O. JONES, and D. R. 
ROGGEN. 1969. On the morphology and 
ultrastruciure of the esophageal region of 
Trichodorus allius Jensen. Proc. Hehninthol. 
Soc. Wash. 36:106-118. 
19. ROGGEN, D. R., D. J. RASKI, and N. O. 
JONES. 1967. Further electron microscopic 
observations of Xiphinema index. Nema- 
tologica 13:1-16. 
20. SAMOILOFF, M. R. 1973. Nematode morpho- 
genesis: pattern of transfer of protein to the 
cuticle of adult Panagrellus silusiae 
(Cephalobidae). Nematologica 19:15-18. 
21. SIDD1QUI, I., and D. R. VIGLIERCHIO. 1977. 
Ullrastructure of the anterior body region of 
marine nematode Deontostoma californicnm. 
J. Nematol. 9:56-82. 
22. WATSON, B. D. 1965. The fine structure of the 
body-wall and the growth of the cuticle in the 
adult nematode Ascaris lumbricoides. Quart. 
J. Micr. Sci. 106:83-91. 
23. WATSON. B. D. 1965. The fine structure of the 
body-wall in a free-living nematode, 
Euchromadora vulgaris. Quart. J. Micr. Sci. 
106:75-81. 
24. WRIGHT, K. A., and W. D. HOPE. 1968. 
Elaborations of the cuticle of Acanthonchus 
duplicatus Wieser, 1959 (Nematoda: Cy- 
atholaimidac) as revealed by light and 
electron microscopy. Can. J. Zool. 46:1005- 
1011. 
25. ZUCKERMAN, B. M., S. HIMMELHOCH, 
and M. KISIEL. 1973. Fine structure changes 
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The Role of Cuticular Strata Nomenclature in the Systematics of Nemata

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