Larval Connectivity and Marine Protected Area Networks

There is growing awareness that ocean life is under unprecedented stress caused by the loss of habitat and biodiversity resulting from human activities. Spatial management by establishing marine protected areas (MPAs) is proposed as an important method to conserve biodiversity, manage fisheries, and increase ecosystem resilience. However, a major challenge in spatial management is that most MPAs and networks of MPAs have been created with little regard to larval dispersal and connectivity within and outside protected areas. Because of the limited understanding of larval connectivity, it is therefore often unclear whether the MPAs are ecologically functional. Larval behavior and dispersal are particularly well studied in benthic crustaceans, making them excellent model organisms to address this challenge.

Response to Visual, Chemical, and Tactile Stimuli

Early life history in marine benthic crustaceans often includes externally brooded eggs that hatch into free-swimming planktonic larvae. These larvae are relatively strong swimmers, and movement in the vertical plane provides a number of advantages, including modulation of horizontal transport and assurance of favorable predator–prey interactions. Swimming behavior in larval crustaceans is regulated by predictable external cues in the water column, primarily light, gravity, and hydrostatic pressure. Light-regulated behavior depends upon the optical physics of seawater and the physiology of light-detecting sensory structures in the larvae, which overall vary little with ontogeny. Swimming in response to light contributes to ecologically significant behaviors in planktonic crustacean larvae, including shadow responses, depth regulation, and diel vertical migration. Moreover, the photoresponses themselves, and in turn the evoked behaviors, change with the needs of larvae as development progresses. Regarding other sensory modalities, crustacean embryos and larvae respond to chemical cues using bimodal sensilla (chemosensory and mechanosensory) as contact receptors, and aesthetascs for detection of water-soluble cues. Processes and behaviors are stimulated by larval detection of chemical cues throughout ontogeny, including egg-hatching, avoidance of predators during free-swimming stages, and, ultimately, settlement and metamorphosis in juvenile habitats. The latter process can also involve tactile cues. The sensory-mediated behaviors described here for crustacean larvae have parallels in numerous arthropod and nonarthropod taxa. Emerging directions for future research on sensory aspects of behavior in crustacean larvae include multimodal sensory integration and behavioral responses to changing environmental stressors.

Organogenesis

This chapter reviews the development of the major organ systems in crustaceans, including musculature, nervous system, circulatory system, digestive system, osmoregulatory system, excretory system, reproductive system, and sensory organs. It describes the morphological unfolding of these organ systems, which generally follows cleavage, gastrulation, and segmentation in the course of ontogeny. Particular emphasis is given to the organ-specific temporal dynamics of development, the onset of functionality, and possible correlations with developmental mode, life history, and ecology. The anatomy and cellular characteristics of developing organs are generally better investigated than aspects of physiology, biochemistry, and molecular biology. Investigations in different crustaceans revealed that the speed of development of the various organ systems varies considerably within an individual and between species. As a rule of thumb, anlagen of the nervous tissue, muscular tissue, digestive system, and excretory organs appear first, followed by the circulatory system. Osmoregulatory organs are formed later. The reproductive organs are the last to emerge and to become functional. The mode of development, behavior, and ecology of the postembryonic stages seem to be major determinants that influence the speed differences of organogenesis. This is reflected by timing differences in development of the digestive system between directly and indirectly developing representatives or species with or without lecithotrophic larvae. Other features of the dynamics of organogenesis suggest evolutionary constraints, such as the delayed development of the nervous system in postnaupliar, relative to naupliar, segments in some species. Mechanistic constraints may be involved in heart development and development of nontransitory osmoregulatory organs.

Settlement and Metamorphosis in Barnacles and Decapods

Settlement and metamorphosis are two crucial processes in organisms with a biphasic life cycle, forming the link between the pelagic larva and benthic juvenile-adult. In general, these processes occur during the final larval stage. Among crustaceans, settlement behavior and the cues that trigger settlement and metamorphosis have been studied in greater depth in barnacles than in decapods, likely a result of the former losing the ability to move after they join the benthic juvenile-adult population, undergoing metamorphosis. Both barnacles and decapods respond to different environmental cues associated with the adult habitat, such as substratum, biofilm, and the presence of conspecifics. In the absence of cues, larvae can delay their metamorphosis for a period of time. This ability to prolong the development can be advantageous because it increases the probability of settling in a suitable habitat. However, delayed metamorphosis has also associated costs (e.g., smaller size, lower growth rate, and higher mortality), which may be carried over to subsequent development stages, with consequences for recruitment.

Hatching

Hatching in crustaceans is an active mechanism in which free, mobile individuals are released from the egg envelopes. For the majority of species, this marks the transition from the embryonic phase of the life cycle, which is spatially constrained by the egg, and the free-living phase. The hatching process of crustaceans has so far not been subject to a detailed comparative treatment across taxa and thus we know little of the diversity of mechanisms, timing in relation to other developmental processes, or evolutionary history. Here we attempt to provide an overview of this diversity throughout the Crustacea. To this end, we treat a particular set of subjects that we consider relevant to the hatching process: the morphology of the involved structures (egg membranes, specialized hatching structures of the hatchling, morphology of the hatchling itself), mechanics of hatchling release, biochemical processes involved in egg shell degradation, maternal and embryonic control and initiation of hatching, as well as the temporal pattern of hatching-related events. A common feature of the hatching mechanism in the majority of crustacean species is an osmotic swelling of the embryo caused by active water uptake prior to hatching, which builds up pressure against the inside of the envelopes. The remaining features vary according to developmental mode and ecological parameters, but the causality behind many hatching-related features remains unclear. However, we conclude that the particular life history strategy can have a strong impact on the relative timing of hatching events.

Duplicated, Twisted, and in the Wrong Place

The study of malformations is an important tool to understand mechanisms and causes of development and regeneration. Moreover, malformations indicate the morphological potential of living beings. Hence, a deeper understanding of how, to what degree, and why organismal structures can deviate from their normal expression is interesting in an evolutionary and ecological context. Like other arthropods, and animals in general, crustaceans show a certain variety of naturally occurring malformations of different body parts. This review is restricted to those that affect the axes of appendages and the trunk. Hence, the various patterns of axis distortion are described and classified. At the general level, malformations concerning limbs are discriminated from those that alter other body outgrowths and those that affect the pattern of the trunk. Among malformation of limbs and other body appendages, misplaced structures, fissions, and fusions are classified. Conjoined twins and distorted body segments are the main features of trunk malformations. The putative causes of malformations are discussed with respect to comparative and experimental approaches. Furthermore, gene expression studies, theories, and models, such as Hans Meinhardt’s Boundary Model, are applied to explain malformations at the level of pattern formation. Apparently, many malformations are not genetic mutations and thus not inheritable, but are instead the result of distortions during early development and regeneration artifacts based on injuries, high temperature, and toxic substances. Compared with other arthropod groups, there are very few experimental studies addressing malformations in crustaceans. Hence, the causes for specific patterns of deformities remain largely obscure.

Dispersal

Dispersal of benthic crustaceans primarily occurs by larvae, which can be transported far from parents. However, larval dispersal is reduced by depth regulation in a sheared water column, where surface and bottom currents flow at different rates or directions, and navigation by postlarvae recruiting to adult habitats. Larvae undertake migrations between adult and larval habitats that range from retention near adult habitats to cross-shelf migrations. The extent of these migrations is regulated by depth preferences and vertical migrations that are timed exogenously or endogenously by diel and tidal cycles over planktonic development. Depth regulation is cued primarily by gravity, hydrostatic pressure, and light, and secondarily by temperature, salinity, and turbulence. Settlement stages navigate to suitable settlement sites using hierarchies of acoustic, chemical, visual, and celestial cues that are effective at different distances. The extent of larval migrations between adult and larval habitats as well as diel vertical migrations may be set by the vulnerability of larvae to abundant planktivorous fish in estuaries and nearshore waters. The timing of larval release and vertical swimming by larvae changes across tidal regimes to conserve migrations between adult and larval habitats across species ranges while minimizing predation.

Effects of Environmental Conditions on Larval Growth and Development

The vast majority of crustaceans are aquatic, living in either marine or freshwater environments. Marine crustaceans—such as copepods, in particular—are ubiquitous in the oceans and perhaps the most numerous metazoans on Earth. Because crustaceans occur in all marine habitats, their larvae are exposed to highly diverse and sometimes variable environmental conditions, including extreme situations in which various environmental factors exert significant effects on larval growth and development. This chapter first describes the effects of food availability on crustacean larvae. Food paucity is a commonly occurring scenario in the wild, which can directly affect larval growth and development and, in severe cases, results in mortality. In the subsequent sections, we cover the effects of temperature and salinity—the two most prominent physical parameters in the aquatic environments—on growth and development of crustacean larvae. We then discuss the influence of other important physicochemical factors in aquatic environments on larval growth and development, including dissolved oxygen, light, ocean acidification, and pollutants. Finally, the last two sections of this chapter discuss synergistic effects of different environmental factors and suggest future research directions in this field.

Patterns of Larval Development

In this chapter, we explore the different patterns of development following the hatching of the crustacean larvae. For many groups of crustaceans, the free-living, postembryonic, and prejuvenile phase is by far the most important part of their life cycle, providing the link between different life modes in successive phases (e.g., between a sessile adult life and the need for long-range planktonic dispersal). Among the aspects covered, we discuss the specific criteria for what a “larva” is, including the necessity for defining specific larval traits that are lacking in other phases of the life cycle. We examine the typical anamorphic and hemianamorphic developmental patterns based on larval examples from a wide selection of groups from Decapoda to Copepoda, Thecostraca to Branchiopoda. In these groups, we examine the most common larval development patterns (including intraspecific variability) of, for example, the zoea, furcilia, copepodite, nauplius, and cypris larvae. We also expand on the importance of the molting cycle as the main driver in larval ontogeny and evolution. Finally, we discuss some of the more general trends of crustacean larval development in light of the general patterns and latest knowledge on tetraconate and arthropod evolution.

Metamorphosis in Crustaceans

Many crustaceans undergo considerable morphological and ecological changes throughout ontogeny. Especially drastic and rapid cases are generally addressed as metamorphosis, which cannot be easily differentiated from nonmetamorphic development; a comparative view is necessary. Evolutionary changes lead to a more metamorphic development either by changing the speed of the developmental process or the morphological difference between earlier and later stages. Five cases of evolutionary changes are differentiated: (1) Skipping stages: An ancestrally gradual developmental pattern becomes more metamorphic as the morphological changes of several molts occur in a single molt; the intermediate stage is skipped. (2) Peramorphosis: A developmental pattern becomes more metamorphic by increasing the morphological difference between early and late stages by “adding” new morphologies to the later part of individual development. (3) Delay and acceleration, single step: A single larval stage becomes delayed in development, more resembling the earlier stage, but differing more strongly from the next stage; hence, this later molt becomes more metamorphic. (4) Delay and acceleration, globally: Several larval stages are delayed in development and hence increase the morphological difference to the later larval stages; this stronger difference is bridged by a single, more metamorphic molt. (5) Caenogenesis: new structures evolve in earlier stages, increasing the difference to later stages; these structures become reduced usually in a single molt, making it more metamorphic. For all cases, examples are presented. Furthermore, terminological issues are discussed, as well as costs and benefits of metamorphic development, followed by a short comparison to insects.