Life History of Alaria marcianae (La Rue, 1917) Walton, 1949 (Trematoda: Diplostomatidae) Author(s): Allen D.

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THE JOURNAL OF PARASITOLOGY Vol. 54, No. 2, April 1968, p. 324-332

LIFE HISTORY ALARIA OF MARCIANAE RUE,1917) WALTON, (LA 1949 (TREMATODA: DIPLOSTOMATIDAE)*
Allen D. Johnsont Department of Zoology, University of Minnesota, Minneapolis
ABSTRACT: The experimental life cycle of Alaria (A.) marcianae (La Rue, 1917) Walton, 1949, involves planorbid snails, Helisoma trivolvis and H. campanulatum, as first intermediate hosts; tadpoles of the leopard frog, Rana pipiens, as second intermediatehosts; mice, rats, and chicks as paratenic hosts; and the domestic cat as definitive host. The life cycle is similar to known cycles in the subgenus Alaria, where avian and mammalianintermediate hosts of the mesocercariaeserve as paratenic hosts; but it differs from the only known cycle in the subgenus Paralaria, where the mesocercariae develop into metacercariae in avian and mammalian intermediate hosts. This difference in mesocercarial behavior represents a distinct biological difference between members of the two subgenera and is an additional subgeneric character. Alaria (A.) minnesotae Chandler, 1954, is a synonym of A. (A.) marcianae (new synonymy).

Six Alaria spp. belonging to the subgenus Alaria Schrank, 1788, have been described from indigenous North American carnivores: A. americana Hall and Wigdor, 1918; A. arisaemoides Augustine and Uribe, 1927; A. oregonensis La Rue and Barone, 1927; A. canis La Rue and Fallis, 1934; A. minnesotae Chandler, 1954; and A. marcianae (La Rue, 1917) Walton, 1949. Of the first five species, Dubois (1963) considered only A. americana and A. arisaemoides valid. Alaria marcianae, the subject of this study, was not included in his revision. From 1960 to 1964, the writer collected adults of an Alaria (A.) sp. from several different carnivore hosts in Minnesota. Additional specimens collected during 1937 and 1938 were available for study. Morphological studies were made of these worms, and the complete life history was studied in experimental hosts beginning with eggs. These parasites were then identified as A. marcianae. REVIEW HISTORICAL La Rue (1917) described the mesocercaria of A. marcianae from the garter snake, Thamnophis marcianus (Baird and Girard) (= T. marciana), and named it Cercaria marcianae. Cort (1918) redescribed this stage collected from tadpoles of the leopard frog Rana pipiens Received for publication 25 September 1967. * Portion of a thesis for the degree of Doctor of Philosophy submitted to the Graduate School, University of Minnesota, 1965. t Present address: Department of Zoology, University of South Dakota, Vermillion, 57069.

Schreber and green frog R. clamitans Latreille, and from the garter snake, Thamnophis sirtalis Cort demonstrated that snakes may (L.). serve as paratenic hosts for the mesocercaria. Cort and Brooks (1928) described the sporocyst and cercarial stages from naturally infected snails, Helisoma trivolvis (Say) and H. campanulatum (Say), and recovered mesocercariae from tadpoles exposed to cercariae. Cuckler (1941) fed mesocercariae obtained from naturally infected leopard frogs to cats from which A. marcianae adults were subsequently recovered. Thus he first established that Alaria spp. require only three hosts instead of four as reported by Bosma (1931) and In the definitive host a Odlaug (1940). tracheal migration occurs involving the transition of the mesocercariae to metacercariae in the lungs before the adult stage is attained in the small intestine. Cuckler also fed mesocercariae to mice and stated that they develop to metacercariae. Although it is evident from an abstract of Cuckler's study (1940) that he was working with A. marcianae, Walton (1949) first formally proposed that Cercaria marcianae be placed in the genus Alaria. The first published description of the adult was provided by Burrows and Lillis (1965) who obtained adults from a naturally infected cat. They identified the adults by comparison with the description in Cuckler's thesis.

MATERIALS AND METHODS four species of planorbid snails, Colonies of Helisoma trivolvis, H. campanulatum,H. corpulentum (Say), and Gyraulus deflectus (Say), were established from egg masses laid by field collected 324

JOHNSON-LIFE HISTORYOF ALARIAMARCIANAE(LA RUE, 1917) (TREMATODA)

325

adults. The age of snails used in experiments was estimated by comparing size with larger, laboratory-rearedadults. Life cycle studies were started with eggs collected by repeated sedimentation of the scraped intestinal mucosa of two striped skunks, Mephitis mephitis (Schreber). Eggs were incubated in distilled water at room temperature. When miracidia appeared fully developed (ca. 20 days), the eggs were put in small vials, covered with cheesecloth, and placed in 10-cm finger bowls containing the snails. Laboratory-rearedtadpoles and frogs were exposed to cercariae singly or in groups of two to four in 10-cm finger bowls. For the recovery of large numbers of mesocercariaefrom infected tadpoles or frogs, the tissues were teased apart and placed on a screen in a funnel containing 0.7% saline. The larvae, free of debris, could be collected in a few ml of saline withdrawn from the funnel. Known numbers of mesocercariae from experimentally infected tadpoles were either force-fed to laboratory-rearedmice and rats and to 1-day-old unfed chicks, or injected intraperitoneally. They were fed to a laboratory-rearedcat in pieces of raw liver and to a parasite-free raccoon in raw eggs. After examination of the tissues of infected mice, rats, and chicks for larvae, the remaining material was ground up in a meat grinder and either artificially digested (0.6% pepsin in 0.35% HC1 at 37 C) or placed on a screen in a funnel containing 0.9% saline (extraction method) for the recovery of additional larvae. The writer collected adults of A. marcianae from the following carnivores examined: 3 of 6 cats; 5 of 10 striped skunks; 1 of 2 spotted skunks, Spilogale putorius (L.); 1 of 10 red foxes, Vulpes fulva (Desmarest); both of 2 gray foxes, Urocyon cinereoargenteus (Schreber); none of 8 raccoons, Procyon lotor (L.); and none of 3 badgers, Taxidea taxus (Schreber). Collection specimens were available from one striped skunk, three spotted skunks, and one badger. Adults used for measurements were fixed without pressure in hot 10% formalin, cleared in methyl salicylate, and mounted in piccolyte. For fixation of cercariae an equal volume of boiling 10% formalin was added to water containing cercariae. Wet mounts of cercariae were prepared for measurements. Sporocysts, mesocercariae,and metacercariaewere fixed in hot 10% formalin. Measurements of sporocysts were from stained and mounted specimens, while those of mesocercariae and metacercariae were from glycerine-cleared specimens. Morphological studies of larvae are based on both living and fixed material. Measurements are given in microns unless indicated otherwise.
RESULTS First intermediate hosts

TABLE I. Results of exposure of snails to eggs of Alaria marcianae. Snail species Helisoma trivolvis
Helisoma campanulatum Age of

snails

Number exposed 30 7 7 17

Number infected
19

1/2

to 3/4

grown 3? grown
% grown 12 grown

7
51 0

Helisoma corpulentum Gyraulus deflectus

1 Sporocysts present but no cercariae shed.

cercariae (Table I). No sporocysts were found in Gyraulus deflectus. Although these results indicate that G. deflectus is not a suitable host for A. marcianae, the status of H. corpulentumr is not clear. Sporocysts developed in five of seven H. corpulentum but no developing cercariae were present in daughter sporocysts even though compared to the other two Helisoma spp. sufficient time was allowed for cercarial development.
Second intermediate host

Seven young adult frogs and 93 tadpoles were exposed to cercariae shed by H. trivolvis and H. campanulatum. No larvae were found in the adult frogs which were killed 10 to 22 days after infection. All tadpoles became infected and fully developed mesocercariae were recovered after 2 weeks. The larvae were present in the thoracic, throat, back, and tail muscles. Most were free in the tissues, although a few larvae were individually encapsulated. After metamorphosis of the tadpoles the mesocercariae in young frogs were found primarily encapsulated in masses ventral to the mylohyoid muscles of the throat, ventral to the sternum and between the muscles of the thighs.
Paratenic hosts

Sporocysts developed in all three Helisoma spp., but none of the H. corpulentum shed

Two rats, three mice, and three 1-day-old unfed chicks were infected with mesocercariae. The animals were killed 7 to 35 days after infection and mesocercariae were recovered from all (Table II). In rats and mice the larvae were observed in the subscapular fat, thigh muscles, abdominal muscles, and the fatty tissues and glands of the throat and jaw region. The larvae in chicks were present in the neck, back, breast, and leg muscles. The larvae in all host species were individually

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THE JOURNALOF PARASITOLOGY, VOL. 54, NO. 2, APRIL1968

TABLE

II. Results of infection of paratenic hosts with mesocercariaeof Alaria marcianae.

No. of larvae given 275 375 280 280 400 400 290 315 Method of infection F F I I I F I I Days after infection 7 35 30 31 31 34 32 34 Method of recovery A A A E E E E E No. of larvae recovered 3 24 2 53 50 27 64 41

Host species rat rat mouse mouse mouse chick chick chick F= I= A= E=

mesocercariae force-fed. mesocercariae intraperitoneally injected. artificial digestion. extraction method.

encapsulated but readily escaped from the cysts in saline. None of the mesocercariae showed any advancement in development. Odlaug (1940) found that mesocercariae of A. mustelae Bosma, 1931, develop to metacercariae in 10 days in mice and rats, so sufficient time was allowed for possible further development.
Definitive host

after the first feeding. No worms were found in the lungs, esophagus, trachea, stomach, or small intestine. Parts of the thigh muscle and the diaphragm muscle were removed and artificially digested but no larvae were recovered.
Description of stages Sporocysts

A young cat was fed 150, 100, and 150 mesocercariae on 3 successive days and was then fed 150 mesocercariae 30 days after the initial feeding. Fluke eggs were first seen in stool specimens 19 days after the initial feeding. The cat was killed 41 days after the initial feeding, and the lungs, trachea, esophagus, stomach, and small intestine were removed and examined separately. The lungs contained 16 metacercariae, and more than 200 worms were recovered from the anterior third of the small intestine. Except for one immature worm, all intestinal forms were sexually mature. It is considered that the adults resulted from the first feedings, whereas the metacercariae and the immature worm resulted from the infection 30 days later. Metacercariae were judged to be fully developed since they were as large as the immature worm from the intestine. A raccoon kept in the laboratory for over 2 years was fed mesocercariae on four different occasions over a period of 7 days with 350, 1,000, 250, and 125 larvae, respectively. Stool specimens from this raccoon at the time it was brought into the laboratory and again a few days before infection were negative for fluke eggs. The animal was killed 19 days

The sporocysts were only briefly described by Cort and Brooks (1928) as elongate, unbranched sporocysts in the digestive gland of infected snails. Description: Mother sporocysts in anterior region of snail hosts, exact location not determined; five specimens from H. trivolvis averaging 14.8 (14.1 to 16.4) mm long by 216 (109 to 306) wide. Birth pore and anterior spines not seen. Germinal masses and daughter sporocyst embryos in sporocyst lumen. Daughter sporocysts (Fig. 5) in digestive gland of snail hosts, 10 specimens from H. trivolvis averaging 1.82 (1.50 to 2.25) mm long by 69 (61 to 82) wide. Spines present at anteriorend and birth pore near anterior end. Germinal masses and cercariae in various stages of development in sporocyst lumen. Cercaria(Fig. 1) Cort and Brooks (1928) described the cercaria but important differences in the spination and additional morphological characters are noted here. Description: (Measurements of 20 specimens from H. trivolvis) Furcocercous, longifurcous, distomate, and pharyngeate. Body, 143 (108 to 190) long by 41 (35 to 49) wide; tail stem, 217 (187 to 245) long by 22 (22 to 25) wide; furcae, 191 (167 to 218) long; oral sucker, 37 (31 to 45) long by 26 (22 to 31) wide; pharynx, 11 (10 to 14) long by 13 (11 to 14) wide; ventral sucker, 22 (20 to 24) long by 22 (20 to 25) wide. Genital primordium midway between ventral sucker and bladder. Unpigmented eyespots mid-

MARCIANAE RUE,1917) (TREMATODA)327 OF HISTORY ALARIA JOHNSON-LIFE (LA

way between oral and ventral suckers laterally. About six pairs of caudal bodies in tail stem. Two pairs of preacetabular penetration glands; ducts opening into oral cavity. Oral hood composed of several rows of staggered spines. Spines smaller and less dense posterior to oral hood, extending to posterior end of body ventrally except for small spineless areas posterior and anterior to ventral sucker; dorsal surface spines extending to level slightly posterior to pharynx, then scattered posterior to ventral sucker and in posterior one-fifth of body. One pair of sensory hairs laterally on posterodorsal surface. Two to four, usually three, rows of scattered spines around ventral sucker. Number of long sensory hairs on lateral margin of tail stem. Two bands of small spines on ventral and dorsal surfaces of tail stem; bands of spines continuing out along ventral and dorsal edges of furcae. Flame cell formula: 2[(2+2+2)+(2+2)+(2)]; bladder bicornuate and lacking an island of Cort. Bladder arms convoluted at level of posterior end

dc
5

bp

Alaria marcianae. Freehand to FIGURES 3-5. scale, from living and preserved specimens. 3. Metacercaria, ventral view. Only major branches of reserve excretory system shown. 4. Mesocercaria, ventral view. Spination shown on right side and primary excretory system on left. 5. Daughter sporocyst. Abbreviations: ac, anterior commissure; bp, birth pore; dc, developing cercaria; eb, excretory bladder; gb, germ ball; gr, genital rudiment; mlv, main lateral vessel; pac, postacetabular commissure; pb, posterior branch; poc, postpharyngeal commissure. of ceca; anterior blind tubule present. Caudal excretory tubule passes medially through tail stem; excretorypores located midfurcally and dorsally.
Mesocercaria (Fig. 4; measurements of 15 specimens from tadpole)

The mesocercaria is essentially an enlarged cercarial body but it lacks the pair of sensory hairs and possesses a more complex excretory system. The flame cell formula is: 2[(2-6+2-6+2-6) +(2-6+2 6)]. The only variation seen from the six flame cells per group was on two occasions when only five were seen. The mesocercaria differs from the description given by Cort (1918) only in possessing anterior and posterior blind excretory tubules and pre- and postacetabularspineless areas. Body 413 (393 to 435) long by 161 (146 to

Alaria marcianae. Freehand to 1-2. FIGURES scale, ventral views. 1. Cercaria, from living and preserved specimens. Spination shown on right side and excretory system on left. 2. Adult, from preserved specimen. Abbreviations: bat, blind anterior tubule; eip,

ejaculatory pouch; la, lappet.

TABLE 3. Species Host ->

-*

Comparative measurements of adults of Alaria marcianae and A. americana in microns.

A. marcianae (after Cuckler, 1941) cat, dog 1.77 (1.28-2.21) 88 (75-102) 82 (66-99) 77 (66-92) 81 (72-99) 118 (99-135) 85 (59-105) length width 535 (402-775) 300 (144-434) 1:0.752 1:1.592 1:0.562 125 70 (118-126) (72-75) 30/100
in feces after Burrows and Lillis, 110 to 127 by 65 to 72, and in present study

A. marcianae (after Burrows and Lillis, 1965) cat

A. marcianae (after Chandler, 1954) cat, Mephitis mephitis (1.45-1.9) (105-114) (diameter) 95 (average diameter) (118-155) (80-111) (480-667) (248-310)

A. marcianae (present study) cat 1.69 (1.57-1.75) 101 (88-122) 95 (82-109) 78 (68-88) 84 (78-95) 126 (112-143) 84 (78-95) 590 (520-690) 200 (160-240) 1:0.80 1:1.64 1:0.35

A. marcianae (present study) Mephitis mephitis 1.66 (1.56-1.84) 105 (95-122) 119 (102-136) 90 (75-109) 109 (88-122) 165 (150-177) 116 (109-136) 620 (540-700) 360 (280-570) 1:0.63 1:1.62 1:0.58 120 (112-129) 72 (65-75) 31/100
from the cat,

A. american (after Hall a Wigdor, 1918 dog

Total length (in millimeters) Oralsucker length width length width

(1.210-1.600) (79-103) (93-114) (74-100) (diameter) (114-150) (78-96) (330-473) (150-233)

(1.16-2.32)

(90-137) (diameter

Ventralsucker Pharynx length width

(70-176) (diameter

(120-196) (80-137)

Holdfast organ

Ratio of lengths pharynx: oral sucker Ratio of lengths hindbody:forebody Ratio of length to width of holdfast organ length Eggs' (uterine) width Position of ventral sucker in forebody
1Eggs of A. marcianae

(90-120) (80-86)

127

(119-140)

feces after Hall and Wigdor, 106 to 134 by 64 to 80, and after La Rue and Fallis, 125 (107-133) 2 Determined here from average measurements. 3 After Dubois, 1938.

by 82 (77-99).

JOHNSON-LIFE HISTORYOF ALARIAMARCIANAE(LA RUE, 1917) (TREMATODA)

329

190) wide; oral sucker, 88 (81 to 95) long by 58 (53 to 67) wide; ventral sucker, 61 (57 to 64) long by 60 (56 to 66) wide.
Metacercoria (Fig. 3)

Cuckler (1941) did not describe the metacercaria but did state that it was similar to that of A. mustelae (see Bosma, 1934). However, of the metacercariae examined here the body shape and also the reserve excretory system were distinctly different from those of A. mustelae. Description: (Measurements of 10 specimens) Typical diplostomulum type metacercaria. Total body length, 656 (593 to 731); forebody width, 363 (304 to 373); hindbody, small, conical, projecting up to 50; oral sucker, 74 (67 to 81) long by 63 (56 to 73) wide; ventral sucker, 64 (59 to 73) long by 64 (59 to 70) wide; pharynx, 50 (46 to 56) long by 42 (36 to 48) wide; holdfast organ, 209 (184 to 238) long by 99 (82 to 109) wide; lappets, maximumlength of 100. Genital rudiment not well differentiated. Bladder enlarged with prominent medial outgrowth extending anteriorly. Bladder arms turning laterad and becoming convoluted near level of anterior end of holdfast organ. Primary excretory system not traced beyond this point. Main lateral vessels of reserve excretory system arising from anterior loop of each bladder arm extending forward to anterior end of body. Laterally each main vessel giving rise to one posterior branch, one or two lateral branches, and one small anterolateral branch. Main posterior branches giving rise laterally to smaller divisions and medially to series of at least six transverse commissures. Entire course of individual commissures could not be followed. Main posterior branches continuing posteriorlybut union not observed. Main lateral vessels giving rise medially to three branches forming, respectively, postacetabular commissure, postpharyngeal commissure,and anteriorcommissure. Median vessel joining three commissures and apparently ending blindly dorsal to holdfast organ. All above branches giving rise to smaller divisions ending blindly in excretory granules.
Adult (Fig. 2)

organ of adults from the skunk was more expanded, often covering part or all of the ventral sucker; and the oral sucker, ventral sucker, and pharynx were larger. Thus ratios involving these structures are different for the two groups of worms. This becomes important when it is recognized that the actual and relative sizes of these structures have been used in distinguishing Alaria spp. (Dubois, 1963). Measurements of adult worms from the different carnivore hosts were similar when the method of fixation and the preparation of whole mounts were the same. Thus the host species did not appear to influence significantly the size of the worms. DISCUSSION Cuckler (1940, 1941) stated that Although mesocercariae of A. marcianae develop to metacercariae in mice, it was definitely established here that they do not advance in development in mice, rats, or chicks. Thus avian and mammalian intermediate host of the mesocercariae are paratenic hosts. The life cycle of A. marcianae is then similar to other known cycles in the subgenus Alaria (see Pearson, 1956, for review of Alaria life cycles). Since a description of the adult of A. marcianae was not published until 1965, comparisons with this species were not included in the descriptions and taxonomic revisions of Alaria spp. Adults of A. marcianae are similar to those of A. canis La Rue and Fallis, 1934; A. americana Hall and Wigdor, 1918; and A. minnesotae Chandler, 1954. All four species possess prominent lappets, a bilobed posterior testis, an ejaculatory pouch, the same anterior extent of the vitellaria, eggs of the same size (Table III), and were described from host species in the same geographical area (northern USA and Canada). In fact, there is no doubt that A. minnesotae is identical to A. marcianae. The adults are similar in size (Table III) and they have been reported from the same host species (cat and striped skunk). Therefore, A. minnesotae is regarded as a synonym of A. marcianae. Dubois (1963) considered A. canis a synonym of A. americana. Both species were described from the dog and, as the brief description of A. americana along with the flattened and contracted condition of the holotype

Burrows and Lillis (1965), and also Cuckler (1941) in his thesis, adequately described the adult, and my measurements of adults given here from a striped skunk and the experimentally infected cat are similar to theirs (Table III). However, certain mensural differences are evident between the adults from the skunk and cat. The worms from both hosts were fixed, and slides prepared, in the same manner, but those from the skunk were dead at the time of fixation. As a result, the holdfast

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THE JOURNALOF PARASITOLOGY, VOL. 54, NO. 2, APRIL1968

makes a critical comparison with closely related species difficult, Dubois' opinion is accepted here. A. marcianae is obviously closely related to A. americana, but differs in (1) its smaller size and (2) its less well developed ejaculatory pouch. The large, thick-walled pouch in A. americana was noted by La Rue and Fallis (1936), by Dubois and Rausch (1950), and by Dubois (1963). I have also observed it in adults from the red fox and the coyote, Canis latrans (Say). It extends almost to the anterior border of the posterior testis and the walls in whole mounts have been reported from 35 to 55 , thick (Dubois and Rausch, 1950; Dubois, 1963). In A. marcianae the walls are about 15 / thick and the pouch extends only a short distance past the posterior border of the posterior testis. The life histories of these two species are alike in that the snail hosts are the same, the cercariae and mesocercariae are similar in size and morphology, and the sporocysts and metacercariae are similar in morphology (see Pearson, 1956, for complete life history of A. americana). However, A. marcianae differs from A. americana in (1) the larger size of the mother sporocysts; (2) the marginal rather than submarginal location of the furcal excretory pores of the cercariae; (3) the more restricted distribution of body spines in the cercariae and mesocercariae (spines cover the entire dorsal surface of both larvae in A. americana); and (4) the smaller size of the metacercariae. Of these differences the spination is probably the more significant, since it is well established in digenetic trematodes that specific morphological differences may be found in larval stages when there is little or no difference between the adults. The division of the genus Alaria into the subgenera Alaria and Paralaria was originally based on the presence of lappets or of pseudosuckers (Dubois, 1938). The diagnoses were later extended to include host specificity (Dubois, 1953). Because pseudosuckers may be evaginated to resemble lappets and the latter invaginated to simulate pseudosuckers, the reliability of these organs to distinguish between members of the two subgenera has been doubted (Webster and Wolfgang, 1956; Dubois, 1963). The basis for this criticism is

evident since these are homologous organs and in certain strigeoids such as A. mustelae Bosma, 1931, both forms have been observed (Dubois, 1963). More recently two additional subgeneric characters were introduced; namely, the shape of the posterior testis and the location of the openings of the forebody gland ducts (Dubois, 1963). This latter character is actually a reflection of the difference in the shape of lappets and evaginated pseudosuckers in Alaria spp. Notwithstanding some criticism, the two subgenera have been retained, and the results here on the behavior of A. marcianae mesocercariae in certain intermediate hosts provide further support for this division. The life cycle of four of the five Alaria (A.) spp. are now known and in all four species avian and mammalian intermediate hosts are paratenic hosts; i.e., hosts in which no advancement in development occurs. Of the four species in the subgenus Paralaria, only the life history of A. mustelae is known, but in this case avian (chicks, personal observations) and mammalian intermediate host are auxiliary hosts; i.e., nonessential hosts in which the mesocercariae develop to metacercariae. This difference in behavior of the mesocercariae represents a distinct biological difference between members of the two subgenera and is an additional subgeneric character. In previous subgeneric diagnoses, members of the subgenus Alaria were considered to be common parasites of canids, but A. marcianae is a common parasite of certain mustelids (skunks) and of cats as reported in this study and also by Chandler (1954). Pearson (1956) reported A. americana from a mustelid, the fisher Martes pennanti (Erxleben), and from certain felids, the lynx Lynx canadensis Kerr and the bobcat L. rufus Schreber. However, since there is definitely an adaptation to the Canidae in the case of the more highly evolved forms in this subgenus (see Dubois, 1944, 1953), host specificity is retained as a subgeneric character. Alaria alata (Goeze, 1782) Krause, 1914, has been reported from canids and a felid (see Sudarikov, 1960), whereas A. arisaemoides Augustine and Uribe, 1927, has been reported only from canids.

JOHNSON-LIFE HISTORYOF ALARIAMARCIANAE(LA RUE, 1917) (TREMATODA)

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Emended diagnosis of the subgenus Alaria Schrank, 1788 (after Dubois, 1963): Lappets present, openings of forebody gland ducts on lateral, striated margin of lappets. Posterior testis multilobed or bilobed. Mesocercariaenot advancing in development in avian and mammalianintermediate hosts (paratenic hosts). Parasites commonly of Canidae, Felidae, and Mustelidae. Type: Alaria alata (Goeze, 1782) Krause, 1914 (see Sudarikov, 1960 for synonyms) Alaria marcianae (La Rue, 1917) Walton, 1949 Synonyms: CercariamarcianaeLa Rue, 1917; Agamodistomum marcianae (La Rue, 1917) Cort, 1918; Mesocercariamarcianae (La Rue, 1917) Olivier and Odlaug, 1938; Alaria minnesotae Chandler, 1954 Alaria americanaHall and Wigdor, 1918 Synonym: Alaria canis La Rue and Fallis, 1934 Alaria arisaemoides Augustine and Uribe, 1927 Synonym: Alaria oregonensis La Rue and Barone, 1927 Alaria nasuae La Rue and Townsend, 1927 Emended diagnosis of the subgenus Paralaria Krause 1914: Pseudosuckers present, openings of forebody gland ducts on distal, striated margin of evaginated pseudosuckers. Posterior testis trilobed, lateral lobes may be subdivided into a dorsal and ventral lobe. Mesocercariae developing to metacercariae in avian and mammalian intermediate hosts (auxiliary hosts). Parasites commonly of Mustelidae. Type: Alaria clathrata (Diesing, 1850) La Rue, 1926 Synonyms: Hemistomum clathrata Diesing, 1850 ex parte; Hemistoma clathratumDiesing, 1850 ex parte Cobbold, 1860; Haemastomum clathratum Diesing, 1850 ex parte Rosseter, 1909 Alaria pseudoclathrata (Krause, 1914) La Rue, 1926 Synonym: Hemistomum pseudoclathratum Krause, 1914 Alaria mustelae Bosma, 1931 Synonyms: Alaria freundi Sprehn, 1932; A. intermedia (Olivier and Odlaug, 1938) Odlaug, 1940; A. dubia Chandler and Rausch, 1946; A. minuta Chandler and Rausch, 1946 Alaria mustelae canadensis Webster and Wolfgang, 1956 Synonym: Alaria canadensis Webster and Wolfgang, 1956 Alaria taxidea Swanson and Erickson, 1946 The host specificity of Alaria (A.) spp. is not due to an ecological segregation of intermediate hosts (see Pearson, 1956, for review of intermediate hosts). One aspect of possible importance may be a difference in the behavior of mesocercariae in different carnivore hosts. For example, certain mustelids may not become infected with A. americana adults simply because the mesocercariae do not advance in

development. Thus, Pearson (1956) reported adults of this species from the fisher and encysted mesocercariae from the ferret, Mustela puttorius (L.) and the otter, Lutra canadensis (Schreber). In this study A. marcianae mesocercariae were fed to a raccoon to determine their behavior in a carnivore in which the adults have not been found, but no larvae lere recovered. ACKNOWLEDGMENT I wish to express my appreciation to Dr. Franklin G. Wallace, adviser for this research, for his suggestions in the preparation of the manuscript. LITERATURE CITED N. BOSMIA, J. 1931. Alaria mustelae sp. nov., a trematode requiring four hosts. Science 74: 521-522. 1934. The life history of the trematode Alaria mustelae, sp. nov. Tr. Am. Micr. Soc. 53: 116-153.
BURRows, R. B., AND W. G. LILLIS. 1965. Trematodes of New Jersey dogs and cats. J. Parasit. 51: 570-574. 1954. New strigeids from CHANDLER, A. C. Minnesota birds and mammals. Am. Midl. Nat. 52: 133-141. CORT, W. W. 1918. The excretory system of

Agamodistomum marcianae (La Rue), the agamodistome stage of a fork-tailed cercaria. J. Parasit. 4: 130-134.

, AND S. T. BROOKS. 1928. Studies on the holostome cercariae from Douglas Lake, Michigan. Tr. Am. Micr. Soc. 47: 179-221. Studies on the migration CUCKLER, A. C. 1940. and development of Alaria spp. (Trematoda: Strigeata) in the definitive host. J. Parasit. 26 (Suppl.): 36.

1941.

Morphological and biological

studies on certain strigeid trematodes of mammals. Ph.D. thesis, Univ. of Minnesota, Minneapolis, 102 p. DUBOIS, G. 1938. Monographie des Strigeida (Trematoda). Mem. Soc. Neuch. Sci. Nat. 6: 1-535. 1944. A propos de la specificite parasitaire des Strigeida. Bull. Soc. Neuch. Sci. Nat. 69: 5-103. 1953. Systematique des Strigeida. ComMem. Soc. plement de la monographie. Neuch. Sci. Nat. 8: 1-141. .1963. Statut des Alariinae Hall et Wigdor, 1918 (Trematoda: Diplostomatidae) et revision de quelques alariens. Bull. Soc. Neuch. Sci. Nat. 86: 107-142. , AND R. RAUSCH. 1950. Troisieme contribution a l'etude des strigeides (Trematoda) nord-americains. Bull. Soc. Neuch. Sci. Nat. 73: 19-50. HALL, M. C., AND M. WIGDOR. 1918. Two new

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flukes from the dog. J. Am. Vet. Med. As. 53: 616-626. LA RUE, G. R. 1917. Two new larval trema-

todes from Thamnophis marciana and Thamnophis eques. Occas. Papers Mus. Zool., Univ. Mich. No. 35: 1-12. , AND A. M. FALLIS. 1936. Morphological study of Alaria canis n. sp. (Trematoda: Alariidae), a trematode parasite of the dog. Tr. Am. Micr. Soc. 55: 340-351. 1940. Morphology and life hisODLAUG, T. 0. tory of the trematode, Alaria intermedia. Tr. Am. Micr. Soc. 59: 490-510. Studies on the life cycles PEARSON, J. C. 1956. and morphology of the larval stages of Alaria arisaemoides Augustine and Uribe, 1927 and

Alaria canis La Rue and Fallis, 1936 (TremaCan. J. Zool. 34: toda: Diplostomidae). 295-387. Suborder Strigeata La SUDARIKOV, V. E. 1960. Rue, 1926. (In: Skrjabin, K. I. Trematodes of animals and man. Moskova, 18: 453-694. Translation: 1965. Israel Prog. Sci. Transl. TT64-11055: 323-495.) A. C. 1949. Parasites of the Ranidae WALTON, XIV. Tr. Ill. State Acad. Sci. (Amphibia). 42: 161-164. WEBSTER,G. A., AND R. W. WOLFGANG. 1956.

Alaria canadensis sp. nov. and Euryhelmis

pyriformis sp. nov. from the skunk Mephitis mephitis in Quebec. Can. J. Zool. 34: 595601.

BOOK REVIEW . . . Animal Agents and Vectors of HlumanDisease by

E. C. Faust, P. C. Beaver, and R. C. Jung. Lea & Febiger, Philadelphia, Third Edition, 1968. ix + 461 p., 186 Figs., 10 Plates, 7 in color. 811.50. This book is a revised edition of a widely used textbook of medical parasitology for preclinical medical students and trainees in the field of public health. The authors state that this edition is thoroughly revised, and enough significant items have been added to justify an essentially new volume. Superficially the third edition looks very much like the second. Upon comparison of the two, however, it is evident that many parts of the text have been revised or rewritten, and one obtains the impression from an incomplete reading that the authors have made every effort to bring the text material up to date and to eliminate superfluities. Remarkably, this has been done with a reduction of the book size by 15 pages. This edition has the same table of contents and general format as the second. Twenty-one chapters cover the subjects of general parasitology, protozoan, and helminth agents of human disease, arthropods as agents and vectors, and technical aids. Adequate author and subject indexes are provided. After a book has gone through three editions one would expect that many technical and publication defects of previous editions have been found and eliminated. This is certainly true of this book. A few minor defects, however, still appear. In the copy for review the new, handsome color plate IV on parasitic amebae is misplaced in chapter 6; it should be in chapter 4. On page ix a book by Whitlock (1960) is listed as a general reference, but a much more useful book on the same general subject by Soulsby (1965) is not. In general most of the illustrations are good to excellent in quality, but a number of unsatisfactory ones remain, for example, Fig. 112f, newly hatched Ascaris larva, and Fig. 124, copulatory bursa of male Tricho-

strongylus orientalis.

This book gives a concise and accurate account of animal agents and vectors of human disease, and provides up-to-date information on antiparasitic medications, diagnostic techniques, and other aspects of medical parasitology. It is a fine textbook on the subject for medical students.

K. C. Kates