Stictodora cablei, Dronen & Blend & Gardner & Jiménez, 2007

Dronen, Norman O., Blend, Charles K., Gardner, Scott L. & Jiménez, F. Agustín, 2007, Stictodora cablei n. sp. (Digenea: Heterophyidae) from the royal tern, Sterna maxima (Laridae: Sterninae) from Puerto Rico and the Brazos County area of the Texas Gulf coast, U. S. A., with a list of other endohelminths recovered in Texas, Zootaxa 1432 (1), pp. 35-56 : 39-45

Stictodora cablei n. sp.

( Figs. 1–3 )

Type host: The royal tern, Sterna maxima Boddaert, 1783 (syn. Thalasseus maximus ), Charadriiformes . Type locality: Puerto Rico, 18° 9’ N latitude, 66° 18’ W longitude. Additional locality: Bryan Utility Lake, Bryan, Brazos County, Texas, U.S.A., 30° 24’ N latitude, 96° 13’

W longitude.

Site of infection: Intestine.

Deposited specimens: Holotype HWML 124830 ; paratypes (2 specimens) HWML 124830 ; vouchers (11 specimens [ HWML 124830 ] and 3 slides of sections [ HWML 124831 ]).

Etymology: The species is named in honor of the late Dr. Raymond M. Cable for his many contributions to our knowledge of the Heterophyidae and the genus Stictodora .

Description: Based on 10 adult specimens (HWML 124830) and sections (HWML 124831). Measurements and comparative morphometric ratios are given in Table 2. With characteristics of genus. Body small, linguiform, anterior 80-85% spinose; forebody about 11% of body length; remnants of cercarial eyespots present near anterior end, absent in some specimens. Mouth subterminal; oral sucker unarmed without appendages; prepharynx long; pharynx longer than wide; esophagus short, approximately 1/5 length of prepharynx; cecal bifurcation approximately 1/4 distance down body near midlevel of forebody; ceca moderately long, terminating about 3/4 distance to posterior extremity. Acetabulum transversely subspherical, with numerous subspherical cells present in main body, approximately equal in size to oral sucker, immediately preequatorial, embedded in parenchyma, highly modified with small pad-like structure at its base surrounded by 3 papilliform arm-like extensions extending sinistral from it, 2 of which (most anterior and most posterior arms) have small plate-like sclerites bearing few minute spines on inner surface; outer edges of all 3 arm-like extensions fused with wall of acetabulogenital sac, supporting wall of sac and genital opening. Testes smooth, located approximately 2/3 down body, approximately equal in size, nearly side by side with left testis slightly ahead of right testis, removed from posterior end by some distance leaving post-testicular space that occupies posterior 1/4 of body. Male terminal genitalia simple, composed of short ejaculatory duct leading posteriorly to oval to round pars prostatica, surrounded by prostate glands, immediately followed by large seminal vesicle composed of 2 distinct divisions; cirrus absent. Acetabulogenital sac immediately sinistral to acetabulum, containing second, larger pad-like structure (gonotyl of Cable et al. [1960]) that extends from left wall of sac; genital opening somewhat sinistral to midline of body on ventral surface. Ovary smooth, subspherical, postequatorial, situated immediately anterior to intertesticular space. Metraterm short, simple, joining with male ejaculatory duct to form simple, non-muscular hermaphroditic duct immediately before entering acetabulogenital sac through posterodorsal wall between small and large pad-like structures (gonotyls). Ootype not observed. Laurer’s canal present, opening not observed. Seminal receptacle posterodextral to midline of ovary and immediately anterior to right testis. Vitelline follicles distributed across most of posttesticular space, from level near posterior margin of left testis to near posterior extremity. Uterus distributed from level of pars prostatica to near posterior extremity, with descending limb passing posteriorly from ovary between testes, reaching posterior extent of vitelline follicles; ascending limb passing behind left testis and to left of ovary; uterine loops overlapping ceca dorsolaterally, approaching body wall in some specimens. Eggs operculate. Excretory vesicle V-shaped, excretory pore terminal.

Remarks. Historically there has been a lack of consensus among researches concerning the placement of heterophyid genera into subfamilies. Stictodora , for example, has been considered to be in Haplorchiinae Looss, 1899 (i.e. Sohn et al. [2003], Travassos [1928], Witenberg [1953]); Galactosominae Ciurea, 1933 (i.e. Price [1934, 1940]); and Stictodorinae Yamaguti, 1958 (i.e. Sogandares-Bernal [1959], Yamaguti [1971]). There are numerous species of Stictodora (see introduction) representing a variety of combinations of morphologies, especially when considering the structure of the acetabulogenital complex. There have been attempts to organize species of this genus. Probably the best know effort was by Yamaguti (1971) who proposed 3 subgenera. Another example of an attempt to divide this large genus into smaller units was proposed by Pearson (1973), who supported the separation of Acanthotrema from Stictodora where species of the former genus have 12 or less spines or sclerotizations in the acetabulogenital complex, a 2 chambered seminal vesicle and lack a prostatic bulb, while species of the latter genus have more than 12 spines in the acetabulogenital complex, a 3 chambered seminal vesicle, and a prostatic bulb.

1 Abbreviations: ACET = Acetabulum; ACETW = Acetabulum width; Approx. = Approximately; BL = Body length; ESOL = Esophagus length; L = Length; OSW = Oral sucker width; PREPL = Prepharynx length; PW = Pharynx length; W = Width.

2 Not given in the published description by Cable et al. (1960); measured from voucher specimen USNPC 038212.

Travassos (1928) described S. acanthotrema (described as Acanthotrema acanthotrema ) from the intestines of the royal tern in Brazil. This original description was minimal and no specimens were illustrated, and although Travassos deposited specimens in the Oswaldo Cruz Institute, Laboratorie de Helminthologia, the museum did not loan out these specimens. Two of us (SG and AJ) examined and photographed the specimens of Stictodora (Acanthotrema) acanthotrema deposited at the Oswaldo Cruz Institute (CHIOC 6090, 6091, 9386); however, these specimens were of marginal quality and provided very little additional information for our comparison of Stictodora cablei n. sp. to this species. Cable et al. (1960) collected a species of heterophyid from the royal tern in Puerto Rico that they felt represented S. acanthotrema and used them to redescribed the species. This redescription was based on 18 specimens; however, only 1 voucher specimen (USNPC 038212) was deposited. Three immature specimens collected by one of us (N.D.) from a royal tern in Bryan, Texas; and 14 whole mounts and 3 slides of sections (unlabeled and unidentified), collected from this same bird host in Puerto Rico and deposited at the HWML (124830.1-13, 124831) by Dr. Raymond Cable, are undoubtedly the same species as the specimen deposited at USNPC (038212) by Cable et al. (1960). These specimens appear to be similar to S. acanthotrema , but they do not match the original description of S. acanthotrema by Travassos (1928) and in our opinion represents a different species of heterophyid, described herein as Stictodora cablei n. sp. Table 2 provides a comparison of the specimens from HWML and the voucher specimen of Cable et al. (1960) (USNPC 038212) to the original description of S. acanthotrema by Travassos (1928). Although S. acanthotrema is almost twice as large as the new species (1,300 –1,400 by 320 compared to 660–860 by 238), has larger testes (112–128 compared to 54–84 wide), and has a larger ovary (96–100 compared to 41–75 wide), Cable et al. (1960) apparently felt that the presence of 3 chitinous hooks (?) in the acetabulogenital complex, a long prepharynx and short esophagus, similar-sized eggs (21–24 by 11– 13 compared to 19–21 by 9–11), and the fact that S. acanthotrema and their specimens were found in the same bird host (royal tern) in the same general region of the world (tropical western hemisphere), suggested that their specimens represented S. acanthotrema . In addition to body size and size of reproductive organs, there are a number of other differences distinguishing the specimens representing S. cablei n. sp. from S. acanthotrema as described by Travassos (1928). Although S. acanthotrema was described as having a long prepharynx and a short esophagus, the ratio of the length of the esophagus to the length of the prepharynx in S. acanthotrema ranges from 1: 1–1: 2 compared to 1:4–1: 10 in S. cablei n. sp. Also, the ratio of the width of the pharynx to body length is 1: 3 in S. acanthotrema compared to 1: 2 in S. cablei n. sp., the ratio of the width of the oral sucker to the body length in S. acanthotrema is 1: 16 compared to 1: 13 in S. cablei n. sp., and the ceca of S. acanthotrema were originally described as being long, reaching to “near the posterior end” of the body, whereas the ceca in S. cablei n. sp. are moderately long, terminating about 3/4 the distance to the posterior extremity. In addition, S. acanthotrema was described as having 3 chitinous hooks extending from the acetabulum into the genital atrium by Travassos (1928), suggesting a structure similar to the “sclerites” found in A. felis by Sohn et al. (2003) or the “genital spines” reported for S. cursitans described by Kinsella & Heard (1974). However, the 3 arm-like extensions of the acetabulum in S. cablei n. sp. do not appear to us to be sclerites or spines, but rather these structures appear in whole mounts and sections as more papilliform structures with a small chitinized plate-like structure bearing spines present on the inner surface of the most anterior arm and the most posterior arm. All 3 arms appear to be fused at one edge to the wall of the genital sac. These structures assume a variety of shapes suggesting that they are more flexible than a chitinized spine-like structure. These papilliform arms appear to serve as rib-like structures that support the wall of the acetabulogenital sac, and assist in the opening of the genital pore (see Figures 2 & 3 ), much like a flower as it opens and closes. Details of the acetabulogenital complex of specimens of S. acanthotrema examined at the Oswaldo Cruz Institute could not be confirmed; however, in one specimen (CHIOC 6090), the acetabulum ( Fig. 4 ) appeared to have at least two blade-like extensions that were much wider and blunter that those of S. cablei n. sp. ( Fig. 3 ), and the genital atrium of S. acanthotrema appeared to be more extensive than that of S. cablei n.sp. It could not be definitely determined if the blade-like extensions of the acetabulum of S. acanthotrema were chitinized, or papilliform as seen in S. cablei n. sp.

For purposes of this study, we have elected to follow Yamaguti (1971) in considering Acanthotrema to be a synonym of Stictodora , and by placing Stictodora in Stictodorinae . Yamaguti (1971) divided species of Stictodora into 3 subgenera: Stictodora where the body is flattened and pyriform, and the eyespots are absent; Galactosomoides where the body is oval, the eyespots are compact and the esophagus is short; and Parastictodora where the body is elongate, the eyespots are disassociated and the esophagus is long. Our specimens are most like those placed in Galactosomoides by Yamaguti (1971) by having the eyespots, when present, “compact” and an esophagus that is much shorter than the prepharynx. Based on our experience with species of Stictodora in this study, we feel that body shape, in particular the distinction between oval and elongate, is not a useful characteristic for separation of this genus into subgroups (subgenera). We also have noted that eyespots are not consistently evident and are quite variable in their distribution in our specimens, which suggests that the presence or absence of eyespots, or their general distribution, may be too variable to be useful as a characteristic to determining subgenera in this genus. In considering the some 30 species that can currently be assigned to this genus, we feel that the length of the esophagus relative to the length of the prepharynx (the relative placement of the pharynx) is a consistent characteristic, and we agree with Sogandares-Bernal (1959) and Yamaguti (1971) that this characteristic is useful in dividing this large group of species into subgroups. Using this characteristic, we have identified 2 subgroups: the sawakinensis -group in which the esophagus is either nearly the same length or longer than the prepharynx (i.e. S. adulecentia ; S. allicoli ; S. caballeroi ; S. cursitans ; S. [ Acanthotrema ] felis (Sohnm Han & Chai, 2003) ; S. fuscata ; S. hainanensis ; S. hancocki ; S. japonica ; S. lari ; S. macrotestis ; S. manilensis ; S. martini ; S. mergi ; S. morosovi ; S. palmifera ; S. perpendiculum ; S. petrowi ; S. pusilla ; S. sawakinensis ; S. sclerogonocotyla ; S. tanayensis ; S. tridactyla ), and the johnsoni -group where the esophagus is much shorter than the prepharynx (i. e. S. acanthotrema ; S. [ Acanthotrema ] armata Lafuente, Roca & Carbonell, 2000 ); S. diplacantha ; S. guerreroi ; S. lariformicola ; S. johnsoni ; S. ubelakeri ). The original description of S. thapari by Witenberg (1953) was based on 1 specimen and it provided no details of the esophageal region of the specimen; however, Witenber’s illustration showed a very long prepharynx, suggesting that this species would be included in the johnsoni -group.

Stictodora cablei n. sp. can be distinguished from all other species in the genus, by having a unique acetabulogenital complex in which the acetabulum is highly modified with a small pad-like structure at its base surrounded by 3 large papilliform arms extending sinistrally, whose outer edges fuse with the wall of the acetabulogenital sac supporting the wall of sac and the genital opening, and where the acetabulogenital sac contains a second, larger pad-like structure (“gonotyl” of Cable et al. [1960]) that extends from left wall of the acetabulogenital sac. The new species has a long prepharynx and a short esophagus and would be placed in the second subgroup. We have not compared the new species to S. diplacantha , S. guerreroi , and S. lariformicola in detail because these 3 species are like S. acanthotrema differentiated above from S. cablei n. sp. by having a prepharynx that is somewhat longer than the esophagus, but where the ratio of the length of the esophagus to the length of the prepharynx is also only about 1: 2 compared to the 1:5–1:10 found in S. cablei n. sp. Stictodora cablei n. sp. can be distinguished from the remaining 4 species in the johnsoni -group as follows: S. armata has 2 large “sclerotized pieces” and a single gonotyl in the acetabulogenital complex; S. johnsoni does not have large sclerotized or papilliform structures, but has a single “gonotyl” present in the acetabulogenital complex; S. thapari has 2 “stout rods” and 2 gonotyls in the acetabulogenital complex; and S. ubelakeri has no large sclerotized or papilliform structures but it has a single gonotyl in the acetabulogenital complex. The new species can be further distinguished from S. johnsoni by having a smaller body (660–825 long compared to 970–1,030), a shorter prepharynx (49–88 compared to 120–280), and a cecal bifurcation that is about 1/4 the distance down the body compared to being at about midbody. It differs further from S. ubelakeri by having a longer prepharynx (55 compared to 22), the ejaculatory duct and metraterm entering the acetabulogenital sac posteriorly rather than from above (anteriorly), the ovary positioned nearly on the midline of the body rather than being directly anterior to the right testis, and S. ubelakeri has a very short (basi- cally absent) esophagus. The new species most closely resembles S. armata in general appearance but differs further from it by having a smaller body size (756 [660–825]) long compared to 1,350 [932–2,100]), a much shorter prepharynx (55 wide, or approximately 7% of body length, compared to 200, or approximately15% of body length), a smaller oral sucker (59, or approximately 8% of body length, compared to 71 wide, or approximately 5% of body length), smaller testes (left testis 69 wide compared to 84; right testis 66 wide compared to 88, approximately 9% of body length compared to 6%), and S. cablei n. sp. is from the royal tern in the New World, while S. armata parasitzes the Audouin’s gull in the Old World.

Additional endohelminths found. In addition to Stictodora cablei n. sp. described above, there were 11 other endohelminthic parasites found in royal terns from Texas, U.S.A.

Figures

FIGURES 1–4. 1. Stictodora cablei n. sp., ventral view of adult. 2. Stictodora cablei n. sp., composite drawing of terminal genitalia and acetabulogenital complex; 3. Stictodora cablei n. sp., photograph of the acetabulum; 4. Stictodora acanthotrema, photograph of the acetabulum. Abbreviations: A, acetabulum; GA, genital atrium; GP, genital pore; LP, large pad; O, ovary; PA, papilliform arm-like structures; SP, small pad; SV, seminal vesicle; T, testis; U, uterus. Scale bars: 1, 170µm; 2, 50µm.