Agarna malayi Tiwari 1952

Aneesh, Panakkool Thamban, Sudha, Kappalli, Helna, Ameri Kottarathil & Anilkumar, Gopinathan, 2018, Agarna malayi Tiwari 1952 (Crustacea: Isopoda: Cymothoidae) Parasitising the Marine Fish, Tenualosa toli (Clupeidae) from India: Re-description / description of Parasite Life Cycle and Patterns of Occurrence, Zoological Studies 57 (25), pp. 1-22 : 3-14

Agarna malayi Tiwari 1952

Agarna malayi Tiwari 1952: 295-300 , pl. iv, text fig. 1-2; Bowman and Tareen 1983, 21; Aneesh et al. 2016a: 1-8, fig. 1 a-d.

Indusa malayi ( Pillai 1964) : 211-223, fig. 3 and 7d; Trilles 1994, 1981; Trilles and Vala 1975

Indusa ophueseni Pillai 1954: 15 .

Host: All the present Indian material is from Tenualosa toli (Valenciennes) ( Clupeidae ). The other host fishes are Nematalosa nasus ( Bloch, 1795) ( Clupeidae ) ( Tiwari 1952) and Mugil ophueseni (Bleeker) (= Valamugil cunnesius (Valenciennes)) ( Mugilidae ) ( Pillai 1954, 1964).

Distribution: Kolkata ( Tiwari, 1952), Travancore ( Pillai 1954), Kayamkulam Lake, Kerala, southwestern coast of India ( Pillai 1964), Bay of Bengal and Malabar Coast of Kerala, India (present study).

Material examined: 55 ññ, 5 transitionals, 50 òò, 4 juveniles, 28 manca I and 36 manca II.

Type material: Holotype: 1 ñ, from Nematalosa nasus , purchased from Bow Bazar, Kolkata, India; Coll. Shri Malay Kumar Datta, Reg. No. C 3121/2 ZSI.

Paratype: 1ñ from Nematalosa nasus , purchased from Bow Bazar, Kolkata, India; Coll. Shri Malay Kumar Datta, Reg. No.C3122/2 ZSI (remaining 5 ññ deposited by Tiwari in 1954 were damaged).

Non-type material: All from Tenualosa toli Ayyikkara Fish Landing Centre (Lat. 11°51'N, Long. 75°22'E; Malabar Coast, India; Coll. Aneesh deposited in PCM. 1 ñ Reg. No. PCM AM-01; 1 ò Reg. No. PCM AM-02; 1 ñ Reg. No. PCM AM-03; 1 ò Reg. No. PCM AM-04; 1 ñ Reg. No. PCM AL-05; 1 transitional Reg. No. PCM AL-23; 1 transitional Reg. No. PCM AL-25; 12 manca I Reg. No. PCM AM-17; 7 manca II, Reg. No. PCM AM-27.

Description ( Figs. 1-13 ): Ovigerous female ( Figs. 1 , 2E, F , 3 , 4 ): Asymmetrical and hunched body, slightly longer than wide, widest at pereonite 4. One side of the body almost straight and other side strongly recurved. Cephalon symmetrical, 1.8- 2 x as wide as long, roughly triangular with narrow round apex, accommodated in the deeply recessed amphicephalic process of pereonite 1. Eyes small, distinct, sub-dorsal and in the posterio-lateral of cephalon. Pereonite 1 without coxa, all the coxae are visible in dorsal view; 2-3 transversely placed, 4-7, triangular, circuitously disposed on antero-lateral surface of the lateral margin and the posterior margin free from the pereonite. All the pereonite except p-1, asymmetrical. Pereonite 1 longest, pereonites 2-3 subequal in length; 4 longer than 3. Pereonite 5-7 decreasing in length progressively, pereonite 7 shortest. The pereonites 1-4 abruptly increase in width towards one side; pereonite 4 widest and gradually decrease the width from 5-7. Pleonites 2-5 visible, increasing progressively in width posteriorly from 1 to 5; pleonite 5 widest and longest. Pleotelson 1.6-1.8 x as wide as long, slightly shorter than pleonite 5, posterior margin broadly rounded. Presence of many pustules on dorsal surface of pleotelson.

Antennule stouter than antenna, composed of 8 articles; articles 4-8 with many setae. Antenna with 9-13 articles, longer and stouter than antennule. Mandible with a well-developed incisor process. Mandible palp 3 segmented and without setae in ovigerous female; basal segment border, apical segment short and conical. Maxillule with 4 unequal slightly recurved apical spines; outer pair much shorter than inner. Bi-lobed maxilla with 2 slightly recurved spines on inner median lobe and two spines on outer lateral lobe. Maxilliped without oostegial lobe; article 3 with 3 large terminal recurved spines.

Pereopods 1-7 without spines; pereopod 1 short and robust, gradually increase in size from 1 to 7, P-7 longest. Pleopods not distinctly visible in dorsal view; pleopod 2 without appendix masculina. Exopodite of pleopod 1-5 without setae. Uropod rami short, flattened extend almost up to the distal margin of pleotelson; rami subequal in length, curved and apically rounded.

Brood pouch with 4 pairs of overlapping oostegites arising from the bases of pereopods 2, 3, 4 and 6; 2nd oostegites small, 4th and 6th large and 3rd medium. Number of eggs or larvae per brood pouch ranges from 110 to 320 according to the size of the female.

Male ( Figs. 2A, B , 5 , 6 ): Relatively smaller than ovigerous female and transitional stage. Body longer than wide and symmetrical, 2.5-2.6 x as long as wide. Cephalon triangular with subtruncate anterior border. Eyes dorsal and larger than female. Pereonite 1 anteriorly trisinuous, anterio-lateral corners slightly produced. Pereonite 1 longest, 2-6 successively shorter. Pereonites 3-5 subequal in width and widest. All the coxae visible in dorsal view, coxae 2-4 more or less equal to pereonite, 5 and 6 longer than pereonite and 7 shorter than pereonite. All pleonites except pleonite 1 visible, increasing progressively in width posteriorly; pleonite 5 widest and longest. Pleotelson as long as wide, slightly shorter than pleonite 5 and distally semicircular.

8 articled antennule stouter and shorter than antenna. Article 2 slightly wider than others. Antennae 9-11 articled, decreasing gradually in width, terminal article with 2-6 setae. Mandible palp 3 segmented, articles 3 with few setae on terminal margin. Maxillule with 4 apical spines slightly recurved; maxilla bi-lobed, with 1 slightly recurved spines on inner median lobe and two spines on outer lateral lobe. Maxilliped without oostegial lobe and a palp with 3 recurved spines on article 3.

Pereopods 1-7 gradually increasing in size, without spines; basis increasing in width progressively. Penes visible on sternite 7. Pleopods not distinctly visible in dorsal view. Pleopod 2 with appendix masculina. Endopodite of pleopods 4 moderately and 5 strongly folded. Uropod rami, nearly reaching the distal margin of pleotelson; rami subequal in length, curved and apically rounded ( Fig. 7 ).

Pereopods 1-7 gradually increasing in size, without spines; Pereopods 1 short and robust, P-7 longest. Pleopods not distinctly visible in dorsal view; pleopod 2 with appendix masculina. Exopodite of pleopod 1-5 without setae. Uropod rami short, flattened extend up to the distal margin of pleotelson; rami subequal in length, curved and apically rounded ( Fig. 7 ).

Transitional ( Figs. 1C, D , 5 ): Body 2.35-2.4 times as long as wide; slightly curved towards one side, Eyes small and moderately distinct. Cephalon partially immersed in poorly developed amphicephalic process of pereonite 1, as long as wide, anterior margin truncate. Pereonites, pleonites, antennules, antenna and mandible palp are similar to those of the ovigerous female and maxilla, maxilliped similar to those of the male. A rudimentary penis is visible on sternite 7. Pleotelson 1.8-2 times as wide as long, slightly wider than pleonite 5 and uropods similar to those of the ovigerous female. Pereopods and pleopods similar to those of female and male.

Juvenile ( Figs. 1H , 8 ): Body approximately 3.3 times as long as wide, relatively narrower and smaller than those of the female, transitional stage and male. Eyes prominent, ovate and conspicuous in dorsal view; anterior margin of cephalon rounded, not immersed in pereonite 1. Pereonite 1 longest, pereonite 2, 3, 4 subequal; pereonite 4 and 5 widest and subequal. Pereonite 5-7 gradually decreasing in length. Pleonites, subequal in length, gradually decreasing in width towards posterior. Pleotelson as long as wide, apical margin rounded with many small reduced setae.

Antennule 8 articled, reaching the anterior margin of pereonite 1; articles 4-8 with few spinules and article 8 with few terminal aesthetics. Antenna longer than antennule, 9 articled, extending to anterior margin of pereonite 2; all the article with few spinules. Article 2 of mandible palp with 2 marginal setae; third article with 3 marginal setae and one apical recurved seta. Maxillule, maxilla and maxilliped similar to those of the male stage.

Pereopod 1-7 with 2-5 spines on posterior margin of propodus; except pereopod 5 and 7 all other pereopod with one spine on the posterior margin of merus. Dactylus of pereopods without tooth and about two times longer than propodus. Penes not developed. The lateral margin of pleopods without setae. Median margin of protopod with 4/5 retinaculae. Pleopod 2 with thick and vestigial appendix masculina, as long as endopodite. Uropod extending beyond the distal margin of pleotelson, inner margin of basis with few setae; rami slightly curved, endopodite relatively large. Endopodite margin few setae. Exopodite few setae, restricted to the inner margin ( Fig. 9 ).

Manca II ( Figs. 1G , 10 , 11 ): Body elongated and transparent, 3.3 times as long as wide, Eyes black, prominent, ovate and prominent in dorsal view. Cephalon 1.5 times as wide as long and golden yellow in colour. Pereonite 1 relatively long; pereonites 2, 3 and 4 subequal in length; longer than pereonites 5 and 6; pereonites 5 and 6 subequal in length; pereonite 7 short and narrow; pereonites 5 widest. All pleonites visible and

(D

subequal in width and length; 4.5 times as wide as long. Pleotelson 1.3 times as wide as long and the apical margin with 40-42 plumose setae.

Eight articled antennule extends to posterior margin of pereonite 1; all the articles with setae and 3-4 spinules and article 8 with four terminal aesthetascs. Antenna longer than antennule, 11 articled, extending to posterior margin of pereonite 2; all the articles with spinules and article 11 with few terminal aesthetascs. Article 2 of the mandible palp with two seta arising from the disto-lateral margin; article 3 with four marginal setae and one apical recurved seta. Maxillule, maxilla and maxilliped similar to those of the male stage.

Six pereopods; pereopod 1-3, with one spine on merus. Dactyls of all the pereopod without tooth. Propodus of pereopod 1-3 broad with 5-6 tooth, 4-6 with few spines. Pleopods not distinctly visible in dorsal view. Pleopod 1 with 20-28 plumose setae on endopodite and 32-36 plumose setae on exopodite. Pleopod 2-5, apical margin of exopodite with 32-36 plumose setae. Uropod rami sub equal, extending strongly beyond the distal margin of pleotelson, curved and apically rounded. Exopodite with 26-28 plumose setae and apical margin with one small and one larger slightly recurved spine; endopodite with 20-22 plumose setae and apical margin with one slightly recurved spine. Uropods and pleotelson with many dark chromatophores.

Manca I ( Fig. 12 ): Body elongated and transparent, 3.8-4.2 times as long as wide, Eyes black, prominent and conspicuous in dorsal view. Cephalon 1.5 times as wide as long, not immersed in pereonite 1. Yolk globules are visible in the pereon, between the pereonites 2 and 6. Pereonite 1 slightly long, pereonite 7 short and narrow. Pereonites 5 widest. All pleonites visible and subequal in width and length; 3.3 times as wide as long. Pleotelson as wide as long, without plumose setae.

Antenna larger than antennule. 8 articled antennule extends to anterior margin of pereonite 2; antenna longer than antennule, 11 articled, extending to posterior margin of pereonite 3; all articles without setae and spinules. Mouthparts are not well developed; mandible palp articles without setae and spines; maxillule, maxilla and maxilliped with poorly developed apical spines. Apical spines not recurved.

Six pereopods; pereopods 1-6 without spines. Distal margin of dactylus of pereopod 1-6 slightly indented and then forming a narrow terminal part. Propodus of pereopod not toothed. Pleopods not distinctly visible in dorsal view. Pleopods 1-5 without plumose setae. Uropod rami subequal, extending strongly beyond the distal margin of pleotelson, apically rounded without plumose setae.

S i z e: Ovigerous female (14-18 mm), transitional (12-15 mm), male (9-13 mm), juvenile (8 mm), manca I (2.4-2.8 mm), manca II (3.4-3.6 mm).

Colour: Male, transitional and female - body white, with scattered faint chromatophores on the dorsal side, more in proximal end of the telson. Juvenile, manca I and manca II- transparent with scattered chromatophores.

Figures

Fig. 1. Photographs of the holotype and paratype of Agarna malayi Tiwari 1952 specimens studied: (A) holotype (C3121/2) dorsal view; (B) holotype (C3121/2) ventral view; (C) paratype (C3122/2) dorsal view; (D) paratype (C3122/2) ventral view; (E) branchial cavity of Nematalosa nasus, showing the holotype (C3122/2) in situ; (F) branchial cavity of Nematalosa nasus, showing the paratype (C3122/2) in situ.

Fig. 2. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes). (A-B) male dorsal and ventral view; (C-D) transitional stage dorsal and ventral view; (E-F) ovigerous female dorsal view; (G) manca II larva; (H) juvenile; (I) ovigerous female on T. toli; (J) manca II on T. toli.

Fig. 3. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes) ovigerous female, (A-B) dorsal view; (C) ventral view; (D) antennule; (E) antenna; (F) mandible; (G) maxillule; (H) maxilla; (I) maxilliped. © 2018 Academia Sinica, Taiwan

Fig. 4. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes) ovigerous female, (A-G) pereopods 1-7; (H) brood; (I) pleopod 2; (J) pleopod 5; (K) uropod; (L) pleotelson and uropods.

Fig. 5. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes) transitional stage, (A) dorsal view; (B) mandible; (C) maxillule; (D) maxilla; (E) maxilliped; (F) pleopod 2.

Fig. 6. Agarna malayi Tiwari 1952 ex Tenualosa toil (Valenciennes) male (A) dorsal view; (B) ventral view; (C) antennule; (D) antenna; (E) mandible; (F) maxillule; (G) maxilla; (H) maxilliped. © 2018 Academia Sinica, Taiwan

Fig. 7. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes) male, (A-G) pereopods 1-7; (H-L) pleopods 1-5; (M) pleotelson and uropods. © 2018 Academia Sinica, Taiwan

Fig. 8. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes) juvenile, (A) dorsal view; (B) antennule; (C) antenna; (D) mandible; (E) maxillule; (F) maxilla; (G) maxilliped. © 2018 Academia Sinica, Taiwan

Fig. 9. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes) juvenile, (A-G) pereopods 1-7; (H) pleopod 2; (I) pleopod 4; (J) uropod; (K) pleotelson and uropods. © 2018 Academia Sinica, Taiwan

Fig. 10. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes) manca II, (A) dorsal view; (B) antennule; (C) antenna; (D) mandible; (E) maxillule; (F) maxilla; (G) maxilliped. © 2018 Academia Sinica, Taiwan

Fig. 11. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes) manca II, (A-C) pereopods 1-3; (D-E) pereopod 5-6; (F) pleopod 1; (G) pleopod 5; (H) uropod; (I) pleotelson and uropods.

Fig. 12. Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes), manca I, (A) dorsal view; (B) antennule; (C) antenna; (D) mandible palp; (E) maxillule; (F) maxilla; (G) maxilliped; (H) pereopod 1; (I) pleopod 2; (J) pleotelson and uropods. © 2018 Academia Sinica, Taiwan

Fig. 13. Schematic representation of the life cycle of Agarna malayi Tiwari 1952 ex Tenualosa toli (Valenciennes); Abbreviations: Manca II (F), manca II at free living stage; Manca II (I), manca II at infective stage; ES, embryonic stage; Fs, female stage. © 2018 Academia Sinica, Taiwan