Ecological, evolutionary, and functional correlates of sensilla number and glomerular density in the olfactory system of decapod crustaceans

Abstract

One of the features common among olfactory systems for vertebrate and invertebrate species is the division of the primary processing area into distinct clumps of synaptic neuropil, called glomeruli. The olfactory glomeruli appear to serve as functional units of olfaction and are the location of the primary processing between chemosensory afferents and second-order neurons. Although glomeruli are found across all phyla, their numbers and size appear to be characteristic for each species, giving rise to the speculation that there is a relationship between glomerular number and function. It has been hypothesized, for example, that animals with more glomeruli may be able to resolve a wider range of odors. Crustacean species are distributed among freshwater, marine, and terrestrial habitats in arctic, temperate, and tropical climates. They also exhibit a variety of lifestyles and behaviors in which olfaction may play a dominant role. Feeding, for example, ranges from carnivorous, through subaquatic and terrestrial omnivorous scavenging, to filter feeding. Mating and territorial behaviors also are known to involve chemical signals. The current study examines glomerular numbers in the olfactory lobes of 17 crustacean species from six of the seven taxa now included in the reptantian decapods. Estimates of the glomerular numbers were obtained from the analysis of sectioned material treated immunocytochemically with an antibody against synapsin that labels proteins contained in neuronal terminals. The numbers of glomeruli found in the different species were then compared with the volume of the glomerular neuropil, numbers of olfactory sensilla, life styles, habitat, and phylogenetic affinities. The picture that emerges from these correlations is that the decapod crustaceans have exploited various strategies in the construction of their olfactory systems in which the problems of size, sensitivity, and selectivity have all interacted. We find a continuum across the groups ranging from those that favor a high convergence of receptor neurons onto a few glomeruli to those that share a small number of receptor neurons among many glomeruli. The potential functional consequences of these differences are discussed.

Comparative brain architecture of the European shore crab Carcinus maenas (Brachyura) and the common hermit crab Pagurus bernhardus (Anomura) with notes on other marine hermit crabs

“…Their analysis strongly suggests that the epitope that SYNORF 1 recognizes is strongly conserved between the fruit fly and the hermit crab. Similar to Drosophila, the antibody consistently labels brain structures in representatives of all major subgroups of the malacostracan crustaceans (see Beltz et al 2003;Harzsch et al 1997Harzsch et al , 1998Harzsch et al , 1999Harzsch and Hansson 2008;Vilpoux et al 2006) in a pattern that is consistent with the assumption that this antibody does in fact label synaptic neuropils in Crustacea. In the crustacean first optic neuropil (the lamina), synapsin labeling is weak compared to the other brain neuropils (Harzsch et al 1997;Harzsch and Hansson 2008).…”

The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships

“…Fibers emerging from these clusters target the core of the neuropil (Fig. 2j), suggesting that these neurons are olfactory interneurons, an arrangement that closely resembles that in Malacostraca (22)(23)(24)(25). We suggest that the remipede clusters D and E correspond to the malacostracan clusters (18) 9͞11 and 10, respectively.…”

“…2h). In Malacostraca, in which these glomeruli have a slightly different architecture, they serve as functional units for olfactory processing and are the sites where the primary chemosensory afferents contact the dendrites of second-order neurons (22)(23)(24)(25). A small additional neuropil, the olfactory satellite neuropil (OS), is located between the ON and LAN1 on both sides of the remipede brain (Fig.…”

Density-dependent effect on reproductive behaviour of Lysmata amboinensis and L. boggessi (Decapoda: Caridea: Hippolytidae)

“…Number of aesthetascs, sensory hair on the outer flagella of the antennules, in L. amboinensis is significantly lower than in the high-density species L. boggessi (D. Zhang, unpublished data). The number of aesthetascs may be associated with the sensitivity of shrimp to distance pheromone (Beltz et al, 2003). Males of L. boggessi with a high number of aesthetascs displayed pre-copulatory behaviour earlier, suggesting that sensitivity of the olfactory system is associated with the number of aesthetascs (D. Zhang, unpublished data).…”