Brain architecture of the largest living land arthropod, the Giant Robber Crab Birgus latro (Crustacea, Anomura, Coenobitidae): evidence for a prominent central olfactory pathway?

Abstract

BackgroundSeveral lineages within the Crustacea conquered land independently during evolution, thereby requiring physiological adaptations for a semi-terrestrial or even a fully terrestrial lifestyle. Birgus latro Linnaeus, 1767, the giant robber crab or coconut crab (Anomura, Coenobitidae), is the largest land-living arthropod and inhabits Indo-Pacific islands such as Christmas Island. B. latro has served as a model in numerous studies of physiological aspects related to the conquest of land by crustaceans. From an olfactory point of view, a transition from sea to land means that molecules need to be detected in gas phase instead of in water solution. Previous studies have provided physiological evidence that terrestrial hermit crabs (Coenobitidae) such as B. latro have a sensitive and well differentiated sense of smell. Here we analyze the brain, in particular the olfactory processing areas of B. latro, by morphological analysis followed by 3 D reconstruction and immunocytochemical studies of synaptic proteins and a neuropeptide.ResultsThe primary and secondary olfactory centers dominate the brain of B. latro and together account for ca. 40% of the neuropil volume in its brain. The paired olfactory neuropils are tripartite and composed of more than 1,000 columnar olfactory glomeruli, which are radially arranged around the periphery of the olfactory neuropils. The glomeruli are innervated ca. 90,000 local interneurons and ca. 160,000 projection neurons per side. The secondary olfactory centers, the paired hemiellipsoid neuropils, are targeted by the axons of these olfactory projection neurons. The projection neuron axonal branches make contact to ca. 250.000 interneurons (per side) associated with the hemiellipsoid neuropils. The hemiellipsoid body neuropil is organized into parallel neuropil lamellae, a design that is quite unusual for decapod crustaceans. The architecture of the optic neuropils and areas associated with antenna two suggest that B. latro has visual and mechanosensory skills that are comparable to those of marine Crustacea.ConclusionsIn parallel to previous behavioral findings that B. latro has aerial olfaction, our results indicate that their central olfactory pathway is indeed most prominent. Similar findings from the closely related terrestrial hermit crab Coenobita clypeatus suggest that in Coenobitidae, olfaction is a major sensory modality processed by the brain, and that for these animals, exploring the olfactory landscape is vital for survival in their terrestrial habitat. Future studies on terrestrial members of other crustacean taxa such as Isopoda, Amphipoda, Astacida, and Brachyura will shed light on how frequently the establishment of an aerial sense of olfaction evolved in Crustacea during the transition from sea to land. Amounting to ca. 1,000,000, the numbers of interneurons that analyse the olfactory input in B. latro brains surpasses that in other terrestrial arthropods, as e.g. the honeybee Apis mellifera or the moth Manduca sexta, by two orders of magnitude suggesting that B....

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

“…The traditional nomenclature of the optic neuropils lamina ganglionaris, medulla interna, and medulla externa has been modified as suggested by Harzsch (2002) to lamina, medulla and lobula. Due to the fact that we could not detect any border between the cell body clusters (9) and (11) of olfactory interneurons as Sandeman et al (1992) mentioned, we restate them cluster (9/11) (see Krieger et al 2010). The term "oesophageal connective" and the corresponding abbreviation OC are maintained here.…”

“…However, the brain anatomy of other Malacostraca, specifically members of the Brachyura and Anomura, has received much less attention in recent years (original contributions on Brachyura, e.g., Rudolph and Spaziani 1990;Schmidt 1997a, b;Sullivan and Beltz 2005a;Sztarker et al 2005Sztarker et al , 2009Wood and Derby 1996;Anomura, e.g., Harzsch and Hansson 2008;Krieger et al 2010;Paul 2003). Brachyura (true crabs) and Anomura (which include hermit crabs) are sister taxa (discussed in Reimann et al 2011) and include representatives that share similar coastal marine habitats and environmental conditions.…”

“…Do closely related species that have highly divergent life styles (such as living in a marine versus terrestrial habitat) display similar brain architecture? This question has recently been explored, e.g., by studying the brains of terrestrial hermit crabs with special respect to their visual neuropils and olfactory lobes (Harzsch and Hansson 2008;Krieger et al 2010).…”

Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world

“…First, stomatopods have a pronounced protocerebral bridge, which is larger than that found in other crustaceans. Secondly, the central body is prominent, and is divided into two parts, as opposed to the singular central body found in other crustaceans such as crabs (Krieger et al, 2010) and crayfish (Utting et al, 2000). Lastly, stomatopods appear to have a pair of small neuropils called the noduli, which are present in many insects but not in any other crustacean investigated so far.…”

“…The brain centres in the eyestalk are connected with the central brain through the protocerebral tracts and optic nerves. Relatively few studies of the crustacean central brain have been undertaken (Chamberlain and Wyse, 1986, Blaustein et al, 1988, Sandeman et al, 1992, Utting et al, 2000, Sullivan and Beltz, 2001a, Harzsch and Hansson, 2008, Krieger et al, 2010, and there is still a lack of knowledge, in particular when it comes to the function of the different regions. Insects on the other hand, have been investigated in numerous studies (Strausfeld, 1976, Strausfeld, 2009b, Strausfeld, 2009a as a few examples), with recent advances in genetic work on Drosophila melanogaster providing a new method of further understanding the circuitry of the brain (Heisenberg, 2003, Olsen andWilson, 2008).…”