Biogeography and Host Usage of Coral-Associated Crustaceans: Barnacles, Copepods, and Gall Crabs as Model Organisms

Most of the diverse groups of crustaceans associated with scleractinian and fire corals form symbiotic relationship with their coral hosts. Coral-associated barnacles include species from the orders Acrothoracica and Thoracica. Most of the coral-associated barnacles belong to the family Pyrgomatidae in Thoracica. Within Pyrgomatidae, the subfamily Ceratoconchinae contains mostly extant species and is present from Florida through the Caribbean to Brazilian waters. The subfamily Megatrematinae has lower species diversity and has a cosmopolitan distribution (except the Eastern Pacific). The Pyrgomatinae are the most species-rich subfamily and distributed only in Indo-West Pacific waters. Host usage of pyrgomatinid barnacles varies spatially, probably related to coral host diversity. Copepods are the most common and most abundant coral-associated crustaceans, often associated with scleractinian, gorgonian, and alcyonacean corals. More than 90% of coral-associated copepods are endemic to the Indo-West Pacific. In contrast, only a few species (<10%) have been discovered from the Atlantic due to several historical perturbations reducing the diversity of their coral hosts. The communities of coral-associated copepods thus show dramatic differences between geographic regions, notably between the Indian, Pacific, and Atlantic Oceans. Brachyurans of the family Cryptochiridae (gall crabs) are obligate associates or parasites, of scleractinian coral hosts in tropical and subtropical seas, being a monophyletic group of only 52 species, from the intertidal to the deep sea (to 512 m) habitats with most (46) recorded in the seas of the tropical Indo-West Pacific and none being cosmopolitan. Atlantic species of Cryptochiridae, apparently not phylogenetically related, display less strict host specificity than their Indo-West Pacific counterparts. Current phylogenetic understandings of the group remain preliminary, while one consistent Indo-West Pacific clade reflects rapid species diversification during the last ~15 million years.

Standing Waters, Especially Ancient Lakes

Crustacea in standing waters are a diverse taxonomic assemblage with representatives in all available habitats from the benthic zone to the pelagial in larger water bodies. While most higher taxa are widespread and occasionally cosmopolitan, this is only partially true at the genus and species level. The crustacean fauna of geologically young lakes, or ponds, is characterized by widespread species that are not even necessarily restricted to lentic habitats. These species generally have good to excellent dispersal capabilities, especially those dwelling in ephemeral habitats. Small groups such as branchiopods and copepods dominate under these conditions among obligate still-water dwellers. In contrast, endemism and occasional striking adaptations are the hallmarks of crustacean species flocks, especially in the radiations of amphipods, decapods, and ostracods in the fewer than 10 ancient lakes worldwide. These radiations have arisen in situ through the diversification of unspecialized ancestors. All comparatively well-studied radiations for which molecular phylogenetic, taxonomic, and ecological data are available show particular adaptations of trophic morphology correlated to specific habitats. Prime examples are the species flocks of amphipods in Lake Baikal and of atyid shrimps in Lake Tanganyika and in two Indonesian lakes. These groups have most likely evolved through adaptive radiation. A major challenge for research on crustaceans in ancient lakes, and in standing waters generally outside Europe and North America, is the lack of basic data from species diversity to genetics for many, if not most, taxa. Getting a grip on species diversity, distributions, ecology, and, at a different level, genomics will be a research priority for coming decades.

Terrestrial Environments

Among crustaceans, only Amphipoda, Isopoda, and Decapoda have invaded truly terrestrial environments, but only two groups show full adaptations to live on land: the family Talitridae among the Amphipoda and the suborder Oniscidea among the Isopoda. The Talitridae occur primarily in forest leaf litter, but a number of other habitats, including caves, are recorded. Talitrids are important ecological contributors to the litter fauna, often occurring in high densities. Their adaptations to a terrestrial way of life include the retention of the mitten-shaped second gnathopods, a neotenic condition among males; the first article of antenna 2 greatly enlarged and fixed to the side of the head; and enlarged gills and pleopods often reduced, sometimes to vestigial stumps. Talitrids have a skewed world distribution being at their most diverse in New Zealand, Tasmania, and Japan/Taiwan. They occur in the Caribbean and Central America but are absent from South and North America except as introduced taxa. Their distribution is largely a result of tectonic activity during the past 150 million years and of extinctions during the Tertiary due to increasing aridity of the climate. The Oniscidea (terrestrial isopods) are the only crustaceans that have managed to adapt to almost all habitat types on land and have become the most species-rich suborder of Isopoda. Although monophyly of the Oniscidea is generally accepted, current taxonomy, based almost entirely on morphological characters, needs extensive revision. Terrestrial isopods present a number of unique adaptations to life on land, some of which result from what can be considered as pre-adaptations of ancestral marine isopods, such as egg development in a marsupium, being dorso-ventrally oblate and having a pleopodal respiration. Other crucial adaptations of Oniscidea include the water-conducting system, the structure of their cuticle, and the “covered” type of pleopodal lungs, all of which are responses to the acute problem of desiccation. They are also among the most speciose taxa in caves, some species have even returned to an aquatic life, and a few species have evolved social behavior. Oniscidea are increasingly being used in biogeographical, phylogeographical, ecological, and evolutionary research and can become model organisms for a broad range of biological studies.

The Fossil Record of the Pancrustacea

Fossils are critically important for evolutionary studies as they provide the link between geological ages and the phylogeny of life. The Pancrustacea are an incredibly diverse clade, representing over 800,000 described extant species, encompassing a variety of familiar and unfamiliar forms, such as ostracods, tongue worms, crabs, lobsters, shrimps, copepods, barnacles, branchiopods, remipedes, and insects. Having colonized nearly every environment on Earth, from hydrothermal vents to terrestrial habitats, they have a diverse fossil record dating back to the Cambrian (540–485 Ma). The quality of the fossil record of each clade is variable and related to their lifestyle (e.g., free-living versus parasitic, benthic versus pelagic) and the degree of mineralization of their cuticle. We review the systematics, morphology, preservation, and paleoecology of pancrustacean fossils; each major clade is discussed in turn, and, where possible, fossil systematics are compared with more recent data from molecular phylogenetics. We show that the three epic clades of the Pancrustacea—Allotriocarida, Multicrustacea, and Oligostraca—all have Cambrian roots, but the diversification of those clades did not take place until the Middle and Late Paleozoic. We also address the potential affinities of three “problematic” clades: euthycarcinoids, thylacocephalans, and cyclids. We conclude by assessing the future of pancrustacean paleobiology, discussing new morphological imaging techniques and further integration with growing molecular phylogenetic data.

Intertidal to Abyss: Crustaceans and Depth

Crustaceans occur from the shelf to hadal depths, but the immense environmental change that occurs along this depth gradient results in significant faunal change. One well-established pattern is the dramatic decline in biomass with depth, a result of an exponential decline in food availability. Average body size becomes smaller, despite observations of deep-sea gigantism in some crustaceans. Crustacean species tend to occupy a limited depth range, resulting in high faunal turnover. The depths of the greatest faunal turnover vary widely throughout the oceans, and there do not appear to be distinct bathymetric “zones” at ocean-wide scales. Molecular research at the species level confirms that small bathymetric changes are often more significant at promoting population differentiation than geographic distance. Observation of crustaceans in the laboratory demonstrates that the interaction between pressure and temperature is likely to act together in limiting the bathymetric range of many species. Debate continues around species richness and diversity gradients, and it remains unclear whether there are more crustacean species on the shelf compared to bathyal depths. Diversity patterns vary between taxa. Decapods are species rich on the shelf and upper slope and less so in the abyss. Isopods show high bathyal diversity, although this pattern varies between regions. For other crustaceans, it is difficult to make generalizations on diversity gradients as there are fewer studies, and results vary depending on geographic region and the method used to estimate diversity and richness. In cumaceans, amphipods. and harpacticoids, species richness is often highest on the shelf, while maximum species diversity occurs in deeper water. Food availability and temperature are good correlates for depth-diversity gradients.

Colonization of Coastal and Estuarine Environments

Coastal and estuarine environments are some of the best-known and most well-studied ecosystems in the world in that these regions lie in close proximity to much of the world’s human population. The crustaceans that inhabit these environments, both as adults and larvae, are adapted to the high productivity that characterizes such areas. We summarize their adaptations and behaviors and the physical characteristics of coastal zones and estuaries in shallower waters (<200 m). In an attempt to objectively review worldwide diversity and endemism within the Crustacea from coastal and estuarine environments, we have used open access global collection data and developed a novel application of an informatics principle (term frequency-inverse document frequency [TF-IDF]) to identify regions with unique faunal assemblages that typify some coastal, shallow waters to assess potential endemism (as assessed by our technique) across groups at differing taxonomic levels. Crustaceans, as a whole, show highest species richness and endemism in three clusters (using the TF-IDF assessment): the eastern temperate north Atlantic, the western temperate north Atlantic, and the western tropical south Pacific. Peracarid and decapod species dominate the collection data, making up 94% of all species analyzed. Peracarids dominate species richness across all temperate zones, yet their highest predicted coastal endemism appears in the eastern north Atlantic by our index. Our analyses using this new method focused on species from less than 200 m depth worldwide. Upcoming impacts of changing sea levels and increases in global temperature will likely have their greatest impact on the fauna of these zones.

Outlook: Crustaceans in the Anthropocene

Since the mid-20th century we have been living in a new geological epoch, Anthropocene, characterized by an overwhelming impact of human activity on the Earth’s ecosystems, leading to mass species extinction by habitat destruction, pollution, global climate warming, and homogenization of biota by intra- and intercontinental transfer of species. Crustaceans are among the most diverse and species-rich animal groups inhabiting predominantly aquatic ecosystems, listed as among the most threatened ecosystems. Global threats include ocean and freshwater acidification, eutrophication, pesticide, hormone and antibiotic load, coastline modification, habitat destruction, overharvesting, and the introduction of invasive species. Many crustaceans are threatened by human-induced modifications of habitats, while others are themselves threats—crustaceans are among the most common invasive species. Those non-indigenous species, when established and integrated, become important components of existing communities, strongly influencing other components directly and indirectly, including by species replacement. They are a threat mostly to species with similar ecological niches, most often to other crustaceans. It is hard to be optimistic about the future of crustacean biodiversity. We may rather expect that growing human pressure will variously further accelerate the non-natural dispersal and extinction rate.

Latitudinal Gradient of Diversity of Marine Crustaceans: TOWARDS a Synthesis

The latitudinal diversity gradient (LDG) is a phenomenon acknowledged for over two centuries. The LDG of marine crustaceans has been studied often but without reaching consensus on its ultimate causative processes. We have undertaken a new synthesis to assess the generality of the LDG and evaluated how potential sampling and other biases, spatial scale, geographic regions, taxonomic aggregation, and differences between clades affect patterns. A meta-analysis of 186 datasets, encompassing 20 studies and 7 crustacean orders, revealed a strong effect size of the species richness-latitude correlation, supporting the existence of a “canonical” LDG. The effect size was sensitive to spatial scale, with studies conducted over shorter latitudinal ranges tending to show a weaker LDG. Correcting for sampling biases in the number of occurrences, taxonomic completeness and spatial heterogeneity did not affect the strength of the LDG, nor did the degree of taxonomic aggregation; effect sizes were similar at family and ordinal levels. However, between orders effect sizes varied strongly, with peracarid orders (Amphipoda, Cumacea, Isopoda) showing a weaker or inverse LDG compared with non-peracarid orders (Calanoida, Euphausiacea, Decapoda, Sessilia). Additional analyses based on a global dataset of >2 million occurrences of >13,000 species revealed patterns undetected by the meta-analysis, including: (1) the existence of a marked bi-modal LDG, with peaks of diversity in subtropical areas (Calanoidea, Decapoda, Sessilia) and in temperate areas (Amphipoda, Isopoda), (2) interhemispheric asymmetry, variable across groups and depths, and (3) ocean basin differences in the shape of the LDG, dependent on taxonomic clade. Both ecological and evolutionary processes play a part. The fossil record of Decapoda showed that its global canonical LDG can be explained by median and range of the age of genera, i.e., hotspots of diversity harbor both younger and older genera and contain a high proportion of genera originating during the Paleogene. In addition, the effect size was negatively related to family age, the LDG being stronger in older families of early Cenozoic and Mesozoic origin. Modes of larval development also played a significant part, taxa without planktonic larvae having weaker or inverse LDG compared with taxa with pelagic larvae. Because clades with direct development tend to show smaller bathymetric and latitudinal ranges than those with pelagic larvae, differences in diversification rates may be implied. Overall, our evidence suggested that the ultimate causes of the LDG are deeply tied to geographic differences in macro-evolutionary rates, i.e., greater rates of species origin and lower rates of extinction in the tropics than in higher latitudes combined with a strong tropical niche conservatism.

What the Ur-crustacean Looked Like

Crustaceans are a paraphyletic assemblage within arthropods. Hexapoda (insects) are nested within crustaceans, with the Remipedia the most likely sister group to Hexapoda. Together, crustaceans and hexapods comprise the monophyletic Tetraconata (also called Pancrustacea). Herein, we “reconstruct” the last common ancestor of crown group Tetraconata, calling it the ur-crustacean. We base our reconstruction on knowledge of extant crustaceans. We tentatively suggest that the ur-crustacean displayed certain characters: The ur-crustacean was a free-living marine species with a distinct head and equipped with two pairs of sensory limbs (antennule and antenna), mandibles, and two more pairs of mouthparts (maxillule and maxilla). We suggest that no further segments were fused to the head and that no maxilliped was present. The ur-crustacean may or may not have possessed a carapace. Its brain was complex, with an extended olfactory system, possibly a central complex, and a lateral protocerebrum containing at least two optical neuropils. The protocerebrum was connected to a nauplius eye as well as to compound eyes. The ur-crustacean might have had a uniformly segmented trunk posterior to its five-segmented head or (less probably) may have possessed two tagmata, a limb-bearing thorax and a limb-less abdomen. It had a heart that might have extended right through the trunk independently of tagmatization. Its thoracopodal appendages were true arthropodal (consisting of podomeres) with a protopod (probably subdivided into coxa and basis), an exopod, and an endopod. Larval development started with a nauplius larva (probably an orthonauplius).

Colonization, Adaptation, Radiation, and Diversity in Fresh Water

About 12,000 of the 67,000 described species of crustaceans occur in fresh water. Crustaceans have colonized almost every type of freshwater environment in most parts of all continents. A common theme in marine-to-freshwater transitions is not only acquisition of osmoregulatory capabilities to cope with hyposalinity, but also optimizing reproductive strategies to cope with ecological and environmental variability. A key reproductive adaptation for fresh water is direct rather than extended planktonic development. Some groups, such as peracarids, were preadapted, already having direct development, whereas others, such as decapods, had to acquire it. Other crustaceans, such as branchiopods, are adapted not only to hyposalinity (and hypersalinity) but also to surviving in transient waters. Crustaceans have been colonizing fresh waters since the Middle Cambrian to Early Ordovician and have independently adapted to life in inland waters many times throughout geological history. The pattern and timing of invasions has shaped present-day distributions. Contemporary distributions and diversity of crustaceans in surface waters are surveyed in the context of their paleohistory. Different groups of crustaceans have very different current distributions that reflect the differential influence of different patterns of colonization, geological history, ecology, and the constraints (or benefits) of their evolutionary heritage.