Functional ontogenetic changes in Branchinecta ferox (Milne-Edwards) (Crustacea: Anostraca)

The development of the anostracan Branchinecta ferox is described in a manner that emphasizes how functional continuity is maintained from the earliest nauplius (1) (length generally < 0.5 mm) to the large adult (length at least 45 mm). The first nauplius subsists on yolk. Feeding begins at stage 2 (2). M orphological specializations of the stage 2 nauplius include the use of a posteriorly located gnathobasic spine on each m andible, a purely naupliar feature, as the sole means of sweeping food particles forward between the mandibles (8, 9). The gnathobasic spines lie across the molar faces which, even if they were sufficiently developed, are therefore debarred from participation in food handling. The self-same mandibular mechanism, based on sweeping and rolling, as persists throughout life is employed. This specialization is restricted to one instar only; at stage 3 the gnathobasic spines no longer lie across the molar surfaces, which are now functional and operate in essentially the same manner as they do throughout life, but at this stage with few of the later refinements. The gnathobasic spines, however, remain as a conspicuous feature of the naupliar mandible (10) and assist the gnathobases throughout the early post-naupliar stages. They persist until an almost complete set of functional trunk limbs has been acquired. The hitherto little-known anatomy of anostracan nauplii has been elucidated, particularly in stages 3 and 4, and is described and illustrated in detail (12-19). Particular attention is given to the complex skeleto-muscular system, whose arrangement is intimately related to locomotion and feeding. Both these activities are analysed. Locomotion is powered entirely by the antennae (20). Because the nauplius is small it inhabits a viscous medium : a low Reynolds number environment. It therefore has no momentum and in effect levers itself through the water with the antennae, whose tips, although having a wide amplitude of beat, actually swing posteriorly for only a short distance during a cycle of movement (21, 22, 24). In the early naupliar stages the return movement of the antennae actually causes the animal to move backward slightly at this phase of the cycle (20, 21). The antennal musculature is described (26). The exopodite spines of the antennae have a purely natatory function. They are not concerned with food collection as some have contended. The antennae are provided with specialized food-collecting spines, the distal masticatory spines (2, 5), which extract particles from suspension as the antennae beat with a frequency exceeding 5 cycles per second at room temperatures. These spines carry food particles to the vicinity of the labrum (20, 25). The labrum is provided with three sets of labral glands whose secretions, stored in conspicuous reservoirs (16, 18, 19), are discharged in a convenient position for entangling collected food particles. The distal masticatory spines are cleaned by setae of the mandibular palps (6) - transient naupliar features - as they leave the vicinity of the labrum (20). Stout, mobile, proximal masticatory spines, located near the base of each antenna (2, 12, 16, 17), sweep material forward to the mandibles. These spines are brush-like from the first feeding stage (nauplius 2) (4), and are bifid from stage 3 (12) until they cease to function at the time the full complement of trunk limbs becomes active. The mandibles pass food to the oesophagus. Post-naupliar development is anamorphic and very gradual. Twenty instars have been identified before the acquisition of a full complement of functional trunk limbs at stage 21 (27). Maxillules and maxillae are added to the mouthparts, and trunk limbs are gradually incorporated into the locomotory/feeding mechanism, usually at the rate of one pair per instar. Such incorporation initially supplements the naupliar mechanism which continues to function until the adult mechanism is fully developed, but different naupliar elements cease to operate at slightly different times (27). There is no simultaneous development of the first six pairs of trunk limbs as has been claimed for Artemia, and no sudden cessation of operation of the naupliar mechanism when six pairs of trunk limbs have become active. Just before the adult system takes over, an almost complete adult mechanism and a naupliar mechanism operate hand in hand. Various aspects of development from the nauplius to the adult are examined, particularly from a functional standpoint, beginning with some consideration of segmentation and early differentiation (28-31). With the assumption of the adult condition, naupliar devices either are lost, as in the case of the mandibular palps, or are transformed, as in the case of the antennae which lose their role in both food handling and locomotion. The antennary glands, a conspicuous feature of the naupliar stages (14, 17, 19), also degenerate to be replaced by the maxillary glands of the adult. Development of the posterior mouthparts (12, 16, 32-34) and of the trunk limbs (33, 35, 36) is described. All these appendages become functional before they achieve the adult condition. Concomitant changes in body form occur as size increases, and the development of other structures, such as the telson (38-41), are noted. In order both to understand functional aspects of the adult and to make intelligible the processes involved in its development, it is necessary to have an understanding of the adult skeleto-muscular system. Its thoracic elements are therefore described in detail, particularly with reference to young adults in which the muscles, being less massive than in large individuals, are less congested (42—50, 57, 61, 62, 65, 70). Although the skeleto-muscular system is complex, its general pattern, which is metamerically repeated in the thorax, can be relatively easily appreciated from illustrations. The development of the muscles is reported (29, 30, 35). The role in the adult of the hitherto little-studied endoskeleton is made clear and the salient features of its development from the early naupliar stages are reported. The nauplius already has a delicate, but complex, endoskeleton on hatching. This gradually extends backwards as an endoskeletal sheet (71) and establishes links with the developing thoracic endoskeleton (47-50). The latter first makes its appearance as a series of intersegmental tendons (28-30) whose subsequent fate is traced. They eventually give rise to a series of struts and sheets (42-46, 49, 57, 61, 62, 70) intimately integrated with the muscles. Besides the major elements of the endoskeleton there are many fibrils and tendon-like sheets, used for suspending or anchoring organs, or load-spreading, as well as fibrils with contractile ends which presumably operate antagonistically to the hydrostatic pressure of the haemocoelic fluid. Examples are illustrated (54-56, 58-62, 65-70, 83). True filter-feeding (as opposed to particle-sieving by the nauplius) begins to be practised for food collection as the trunk limbs gradually come into service. Aspects of this process in the early post-naupliar stages are described and certain points concerning filter-feeding in young adults are discussed. The trunk limbs beat with a metachronal rhythm . The sequence within the series, and the cycle of motion of a single appendage, are described (76-78), previously unreported subtleties of these processes being reported. Notwithstanding claims to the contrary, made for other anostracans, no forwardly directed current appears to flow in the food groove. Food is moved forward mechanically by the tips of the proximal gnathobasic setae which, from an early stage of development, are specialized for this function (36, 79, 84, 95-98). The feeding mechanism of young adults is briefly described. Contrary to certain statements in the literature, the maxillules and maxillae, especially the former, while small, are not vestigial. The maxillules fulfil a vital role in transferring food to the mandibles from the region to which it is swept by the gnathobases of the first trunk limbs. While much food consists of suspended particles, material is also scraped from substrata by means of denticulate spines of the trunk limb endopodites (122-126). But this means large amounts can sometimes be collected quickly. Certain glands, located near the base of each trunk limb, and others in the gnathobases of the limbs, are briefly described (79). Filter-feeding by means of finely spaced filtering setules on the trunk limb filter setae continues until the animal attains a length of about 18 mm. Subsequently, over a very small number of moults, the endite armature of the trunk limbs is transformed. The finely spaced filtering setules (84-89) are replaced, first by somewhat more widely spaced setules (91), then by stouter, m uch more widely spaced structures which make up a coarse grid (92-94), and are finally lost entirely (99-101). These changes are accompanied by a drastic change in feeding habits. Hitherto a feeder on algae and particulate detritus, B.ferox becomes a carnivore. In at least one area in the Middle East the food consists largely of the calanoid copepod Arctodiaptomus similis, but the cladoceran Daphnia atkinsoni bolivari and other prey are also eaten. Transformation of the entire armature is accompanied by changes in the endopodite spines which lose their scraping function (128-138). Concom itant changes take place in the labral glands. In the filter-feeding adult stages there are three sets of glands, the direct descendants of those of the nauplius, each with its own secretion-filled reservoir and exit duct (83). These degenerate after the animal has ceased to filter, and no secretions are produced from this source in large carnivorous individuals. The trunk limbs of the post-filter-feeding stages, armed medially by the now stout endite spines, make up a median cage (133) into