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). Morphological specializations of the stage 2 nauplius include the use of a posteriorly located gnathobasic spine on each mandible, 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, much 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). Concomitant 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 which prey is sucked by currents set up as in the filter-feeding stages. Such prey is forced into the food groove and passed forward mechanically by the stout gnathobasic spines (112-120), thence, via the maxillules, to the mandibles as in the filter-feeding stages. No forwardly directed current in the food groove is involved. The last pair of trunk limbs, which differ from the rest (133, 136), fence off the median chamber posteriorly. From the stage 3 nauplius, when they first begin to handle food particles, the molar surfaces of the mandibles are elaborated to render this process more efficient. This elaboration increases and becomes very complex during the filter-feeding stages. Efficiency is increased by mandibular asymmetry (148). Each molar face has a series of more or less dorso-ventrally running ridges subdivided transversely into teeth, each produced into several cusps (153). The molar surface on the right mandible develops a groove dorsally. This is bounded by stout spines and in its depth are toothed ridges, each tooth bearing several cusps. Both the marginal spines and cusped teeth change in form with increase in size (155, 156, 163, 164, 168, 169). Dorsally on the left mandible is a series of stout teeth (159, 160) which fit into the groove of the right molar surface to produce a crushing and triturating device. The ventral margins of the molar surfaces are armed with specialized spines (166, 167, 172-174) which both fence off the triturating regions and assist in the sweeping of food particles. By the time the animal is approaching the end of the filter-feeding phase these make up a complex array (182-184). In large, carnivorous adults the molar surfaces are somewhat less elaborate and are crushing structures (180, 181). Large posterior teeth are also developed on both mandibles (149, 150) - one of the few cases where rolling and sweeping branchiopod mandibles have acquired a biting capability. The right mandible also loses the teeth within the now enlarged groove, and the adjacent marginal teeth become reduced in number but increase in robustness. It is stressed that the pattern of development is one of strict anamorphosis. There is no sign of the development of the first six pairs of trunk limbs as a unit whose members become functional simultaneously and which, as a mechanism of the adult-type, suddenly replaces the naupliar swimming and feeding mechanisms at this stage. Claims that this is so in the Anostraca appear to be erroneous. No such metamorphosis occurs in B. ferox, and evidence culled from the literature shows that the condition in this species is typical of anostracan development as a whole. Previous suggestions that the anostracan pattern of development is less primitive than that of the Cephalocarida are therefore untenable. In this respect there is nothing to support the suggestion that either group is more primitive than the other. While we now have a reasonable idea of the major features of anostracan development from the nauplius to the adult, both in terms of gross morphology and for some of the major organ systems, we have little idea how this pattern is established and controlled. Certain hypothetical developmental models, not proposed with the Anostraca in mind, are interesting but contribute hardly at all to our understanding of morphogenesis. Possible lines of attack are briefly mentioned. The stages between the nauplius and that stage at which all the adult appendages become functional can to some extent be regarded as motile embryos. Processes that take place in the embryo of many organisms - somite formation and the development of limbs - do so in a motile organism that has by its own efforts to maintain the energetic demands of growth and differentiation. That the Anostraca have been successful in this respect is indicated by their long survival and their enormous geographical range in a variety of climates, albeit in a restricted range of habitats which, however, include many that call for great ecological or physiological tolerance. The entire life cycle of B. ferox is enacted in a single water body. Selective forces must act in very different ways on small nauplii and large adults with their different morphologies and functional needs, yet presumably do so in similar ways so far as basic physiology is concerned. The very different morphological specializations of the various stages are therefore probably accompanied by wide eco-physiological tolerance. Such a pattern is very different from that of many animals whose juvenile and adult stages differ much in morphology, each being specialized for a particular way of life and occupying niches that are not only very different but which are found in quite different environments. Such tolerance has probably contributed to the long survival of the Anostraca and probably assisted Artemia in the initial stages of its colonization of hyper-saline environments. B. ferox reveals the potentialities inherent in an organism that retains two primitive attributes, anamorphic development and the retention by the adult of a substantial degree of serial homology.