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<I>Nerocila Acuminata</I> (Isopoda, Cymothoidae)

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<I>Nerocila Acuminata</I> (Isopoda, Cymothoidae) BULLETIN OF MARINE SCIENCE, 41(2): 351-360,1987 BEHAVIOR OF JUVENILE NEROCILA ACUMINATA (ISOPODA, CYMOTHOIDAE) DURING ATTACK, ATTACHMENT AND FEEDING ON FISH PREY Earl Segal ABSTRACT Juvenile Nerocila acuminata are blood and tissue feeders which, under laboratory condi- tions, show no prey specificity attaching to and feeding upon Menidia beryllina (silversides), Cyprinodon variegatus (sheepshead minnow), Mugil cephalus (mullet), Fundulus similis (kil- lifish), Trachynotus carolinus (pompano), Lagodon rhomboides (pinfish), and Anchoa mitchilli (anchovy) from the Gulf of Mexico. Attacks occurred either in mid-water or from the bottom. In mid-water, isopods would swim in from the rear, on any compass setting, adjusting their dorso-ventral swimming orientation to land with outstretched pereopods, Speed adjustments were precise since, in over 50 attacks, overshooting did not occur. From the bottom, isopods which were lying on their backs with the first three pairs of per eopods extended, either hooked a slowly passing fish or flipped their pleopods and propelled themselves onto a fish. Thus, juvenile N. acuminata are behaviorally equipped to attack either pelagic or demersal fishes. Undamaged fish did not respond overtly either to the sight of or transient contact with the isopods; damaged fish took evasive action. If attachment occurred on the body rather than on the fins, the fish responded with a variety of dislodgment tactics the vigor of which diminished with additional attachments. In the isopod family Cymothoidae all known species appear to be pelagic while young (Williams, 1984) and either parasitic or commensal as adults when they take up residence on host fish by one of three modes: by attaching to the surface; by entering the gill chamber and/or buccal cavity; or by burrowing under the epidermis. Recently, Brusca (1981) has monographed the Cymothoidae of the eastern Pacific while offering extensive insights into the developmental and life histories, host parasite relations and ecological ramifications of host specificity of various species. Almost all the available information concems the adults; juveniles are poorly known and their relationships to their hosts or prey are little understood. A fortuitous collection of juvenile Nerocifa acuminata Schioedte and Meinert 1881 from the Gulf of Mexico offered an opportunity for a detailed descriptive study of various aspects of their behavior while swimming, feeding and interacting with their prey. In a more limited way it presented a situation for observing the responses of prey to small predators, a subject Barlow (pers. comm.) feels has been sadly neglected. Since juvenile N. acuminata will be shown to be temporary blood feeders I consider them to be micropredators rather than parasites making the same dis- tinction Marshall (1981) does when comparing Diptera that land on their hosts to take a blood meal then flyaway with those that spend their lives on their hosts whether they feed or not. Thus fish upon whom juvenile N. acuminata feed are their prey. MATERIALS AND METHODS From 10 December 1961 through 19 May 1962, 8 I juvenile Nerocila acuminata Shioedte and Meinert, 1881, were collected in seine hauls from an isolated shallow lagoon to the west side of the Houston ship channel jetty on Galveston Island, Texas. Collections were made on 10 December (-60 specimens), 17 December (3), 25 January (15 collected, 10 recovered), 8 May (I) and 19 May (2). The last collection on 19 May was from a smaller back beach lagoon which received some fresh water 351 352 BULLETIN OF MARINE SCIENCE. VOL. 41. NO.2. 1987 over and through the ship channel wall. Systematic attempts to obtain additional N. acuminata over the following1.5years and isolated attempts over the next 15years were unsuccessful.In the aftermath of hurricane Carla, which hit the Texas coast during the fall of 1961,a buildup of sand occurred along the beaches and in the lagoons on Galveston Island progressively blocking entrances and cutting off water exchange.With the warming of the shallow lagoon water during the spring and summer of 1962 (33°Con 19 May in the isolated lagoon)Sargassum sp., which had accumulated during the hurricane, died and decayed, effectivelykilling the lagoons. When the animals were captured the majority had a bright red gut. Numerous fish (see Results) were seined with the isopods but on no occasion were the isopods found on the fishin the seine. Both isopods and fishwere returned alive to the laboratory at Rice University in Houston and housed apart in aquaria and plastic boxes. All fish collected with the juvenile N. acuminata were young and adults of small species,e.g., Cyprinodon variegatus, Fundulus similis and Menidia beryllina or youngoflarger species, e.g., MugU cephalus and Trachynotus carolinus. Becauseof limitations in laboratory holding space, no attempt was made to procure larger fish from the lagoon. Both isopods and fishes were maintained and tested at 15°Cand 280/00sal. in natural lagoon water (conditions under which the animals were collected).All observations of and arranged interactions between isopods and fish were carried out with one primary objective-to record the actions of livingjuvenile cymothoid isopods. Responses of the prey were noted. RESULTS External Features. -Figure IA illustrates the dimensions and shape of a repre- sentative juvenile Nerocila acuminata. The eyes are large, oval and curved around the sides of the head. This is characteristic offree swimming, juvenile cymothoid isopods. In every individual there are a minimum of two rows of ommatidial facets on the ventral surface of the head. The uropods, pleopods and pleotelson all possess plumose marginal setae. All seven pairs of pereopods are prehensile, terminating in long, narrow, curved dactyli. Pigmentation is extensive, consisting of myriad aggregations of starburst shaped chromatophores. Size. - Of the 13 juveniles subsequently available for measurement, the largest was 18.6 mm (L) by 5.1 mm (W) with a body index (L-W) of 3.65 while the smallest was 12.8 mm (L) by 3.9 mm (W) with a body index of 3.28. However, body indices ranged from 3.28 to 3.95 with an X of3.58 and no discernible trend of body index with body size. Non-prey Oriented Behavior. -SWIMMING. As swimmers the animals were re- markably graceful and adroit. They swam rapidly in a straight line interspersing loops, half immelmans and turns. They normally swam ventral side down but occasionally switched to dorsal side down for short distances when they reversed direction after bouncing off an obstacle, e.g., a fish or the sides of the aquarium (Fig. 2A). On no occasion did the isopods avoid an obstacle by changing course before contact. Upon contact they either looped upward or downward and headed in the opposite direction. Or, the animals turned to either side, on the horizontal or the oblique, and continued on whatever angle their turns took them. Much of the swimming appeared to be random and non-prey oriented. NON-SWIMMING. Periodically the animals would glide to a halt on the bottom, ventral side down. After a few seconds to a few minutes they would resume swimming with the same dorso-ventral orientation. Occasionally isopods settled on the bottom, ventral side up. Since this invariably led to an attack it will be presented below. Molting, with cessation of swimming and feeding, also took place on the bottom. Nine individuals attached by the first three pairs of pereopods to any available bottom projection. Three remained in the original attachment location; two for 3 and one for 4 days. The latter completed the molt and resumed swimming. All others either died or disappeared and were presumably eaten. SEGAL: BEHAVIOR OF JUVENILE NEROC/LA ACUM/NATA PREYING ON FISH 353 Figure IA. Representative, free swimmingjuvenile Nerocila acuminata with characteristic large eyes, streamlined shape and pereopods ending in long, curved dactyli. Figure lB. Menidia beryl/ina (silverside) hosting 10juvenile N. acuminata (three individuals on right side). All isopods arc oriented in the same direction. Dark gut of isopods indicates feeding. Prey Oriented Behavior. - Isopod attacks took place either while both parties were swimming or when a fish swam slowly over an isopod which was lying on the bottom, ventral side up. In the swimming mode, isopods always approached from the rear, maintaining in the dorsal position, or assuming in all other positions, an appropriate attachment orientation. Thus, an isopod coming in from above would, depending upon its approach speed, either glide in or spurt in on the dorsal or dorsolateral surface; an isopod approaching from below would reorient 1800 on its axis and come in ventrally (Fig. 2B). From any other compass orientation 354 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987 Figure 2A. (Left) Non-feeding contact behavior of N. acuminata and potential prey fish. Figure 2B. (Right) Mid-water attack behavior of juvenile N. acuminata. Attacks were always from the rear either above, below or to the sides of the fish. an isopod would tilt accordingly and swim in on the flank. Speed adjustments appeared to be precise since of the more than 50 observed swimming attacks not one resulted in an overshoot. Whether an attack resulted in an attachment de- pended, in good part, on the response of the prey (see below). In the bottom attack the isopod played a relatively passive role. Lying on its back with limbs extended it could hook, with its first three pairs of pereopods, any accessible region of a slowly passing fish. Occasionally, when contact had not been made, an isopod would flip its pleopods and propel itself onto the fish. Invariably, a bottom attack resulted in attachment to an anal fin (Fig. 2C). If an attack was successful an isopod did not necessarily remain at the site of attachment. Isopods were capable of crawling over the surface to the degree that no area of a fish was inviolate.
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