Transition from marine to terrestrial ecologies: Changes in olfactory and tritocerebral neuropils in land-living isopods

The European shore crab Carcinus maenas and the common hermit crab Pagurus bernhardus are members of the sister taxa Brachyura and Anomura (together forming the taxon Meiura) respectively. Both species share similar coastal marine habitats and thus are confronted with similar environmental conditions. This study sets out to explore variations of general brain architecture of species that live in seemingly similar habitats but belong to different major malacostracan taxa and to understand possible differences of sensory systems and related brain compartments. We examined the brains of Carcinus maenas, Pagurus bernhardus, and three other hermit crab species with immunohistochemistry against tyrosinated tubulin, f-actin, synaptic proteins, RF-amides and allatostatin. Our comparison showed that their optic neuropils within the eyestalks display strong resemblance in gross morphology as well as in detailed organization, suggesting a rather similar potential of processing visual input. Besides the well-developed visual system, the olfactory neuropils are distinct components in the brain of both C. maenas and P. bernhardus as well as the other hermit crabs, suggesting that close integration of olfactory and visual information may be useful in turbid marine environments with low visibility, as is typical for many habitats such as, e.g., the Baltic and the North Sea. Comparing the shape of the olfactory glomeruli in the anomurans showed some variations, ranging from a wedge shape to an elongate morphology. Furthermore, the tritocerebrum and the organization of the second antennae associated with the tritocerebrum seem to differ markedly in C. maenas and P. bernhardus, indicating better mechanosensory abilities in the latter close to those of other Decapoda with long second antennae, such as Astacida, Homarida, or Achelata. This aspect may also represent an adaptation to the "hermit lifestyle" in which competition for shells is a major aspect of their life history. The shore crab C. maenas, on the other hand seems to rely much less on mechanosensory information mediated by the second antennae but in water, the visual and the olfactory senses seem to be the most important modalities.

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“…Scale bars 0 100 μm. Note that b is modified from Harzsch et al 2011 The deutocerebrum of other anomuran species…”

Section: Tritocerebrummentioning

confidence: 99%

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

et al. 2012

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“…In some decapods crustaceans, these glomeruli may be extremely elongated [8,10], whereas studies on representatives of the basal malacostracan taxon Nebalia (Leptostraca) suggest spherical glomeruli to be part of the malacostracan ground pattern (Kenning and Harzsch; unpublished results). Such spherical glomeruli are also present in marine Isopoda [9]. Furthermore, it has been well documented from crayfish (Astacidea), spiny lobsters (Palinuroidea) and hermit crabs (Paguroidea) that in the olfactory lobe each glomerulus is stratified and provides an outer cap, a subcap, and a base [8,10,34].…”

Section: Introductionmentioning

confidence: 99%

Comparative analysis of deutocerebral neuropils in Chilopoda (Myriapoda): implications for the evolution of the arthropod olfactory system and support for the Mandibulata concept

et al. 2012

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BackgroundOriginating from a marine ancestor, the myriapods most likely invaded land independently of the hexapods. As these two evolutionary lineages conquered land in parallel but separately, we are interested in comparing the myriapod chemosensory system to that of hexapods to gain insights into possible adaptations for olfaction in air. Our study connects to a previous analysis of the brain and behavior of the chilopod (centipede) Scutigera coleoptrata in which we demonstrated that these animals do respond to volatile substances and analyzed the structure of their central olfactory pathway.ResultsHere, we examined the architecture of the deutocerebral brain areas (which process input from the antennae) in seven additional representatives of the Chilopoda, covering all major subtaxa, by histology, confocal laser-scan microscopy, and 3D reconstruction. We found that in all species that we studied the majority of antennal afferents target two separate neuropils, the olfactory lobe (chemosensory, composed of glomerular neuropil compartments) and the corpus lamellosum (mechanosensory). The numbers of olfactory glomeruli in the different chilopod taxa ranged from ca. 35 up to ca. 90 and the shape of the glomeruli ranged from spheroid across ovoid or drop-shape to elongate.ConclusionA split of the afferents from the (first) pair of antennae into separate chemosensory and mechanosensory components is also typical for Crustacea and Hexapoda, but this set of characters is absent in Chelicerata. We suggest that this character set strongly supports the Mandibulata hypothesis (Myriapoda + (Crustacea + Hexapoda)) as opposed to the Myriochelata concept (Myriapoda + Chelicerata). The evolutionary implications of our findings, particularly the plasticity of glomerular shape, are discussed.

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“…Terrestrial hermit crabs (family Coenobitidae, genus Coenobita; [34]) spend the majority of their lives on land, and only their larvae spend extended periods in water (Coenobitidae are terrestrialized to level G4, sensu Greenaway, 2003). Unlike most other terrestrialized malacostracans, coenobitids are adept at sensing and tracking airborne odours [35][36][37]. Coenobitid crabs have antennules bearing aesthetascs that differ in morphology from the hair-like aesthetascs of aquatic malacostracans [38][39][40].…”

Section: Chemosensory Antennules Of Terrestrial Hermit Crabsmentioning

confidence: 99%

“…Like coenobitid crabs, insects are adept at tracking odour plumes in air [57]. Insects have lost their first antennae and secondarily developed chemosensory sensilla on their second antennae, thus the olfactory capture structures of coenobitid crabs and insects are not homologous [35,36]. Studies of sniffing by insects in air are few.…”

Section: Comparison To Other Terrestrialized Members Of Tetraconata (mentioning

confidence: 99%

“…One exception to this is terrestrial isopods, which exhibit weak olfactory-guided behaviour in air; their antennules are reduced in size and number of aesthetascs compared with those of aquatic isopods [56]. Desert isopods lack aesthetascs, do not flick their antennules and the areas of the brain responsible for processing olfactory information have been functionally lost [36]. Like coenobitid crabs, insects are adept at tracking odour plumes in air [57].…”

Section: Comparison To Other Terrestrialized Members Of Tetraconata (mentioning

confidence: 99%

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Do terrestrial hermit crabs sniff? Air flow and odorant capture by flicking antennules

Waldrop

Koehl

2016

J. R. Soc. Interface.

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Capture of odorant molecules by olfactory organs from the surrounding fluid is the first step of smelling. Sniffing intermittently moves fluid across sensory surfaces, increasing delivery rates of molecules to chemosensory receptors and providing discrete odour samples. Aquatic malacostracan crustaceans sniff by flicking olfactory antennules bearing arrays of chemosensory hairs (aesthetascs), capturing water in the arrays during downstroke and holding the sample during return stroke. Terrestrial malacostracans also flick antennules, but how their flicking affects odour capture from air is not understood. The terrestrial hermit crab, Coenobita rugosus, uses antennules bearing shingle-shaped aesthetascs to capture odours. We used particle image velocimetry to measure fine-scale fluid flow relative to a dynamically scaled physical model of a flicking antennule, and computational simulations to calculate diffusion to aesthetascs by odorant molecules carried in that flow. Air does not flow into the aesthetasc array during flick downstrokes or recovery strokes. Odorants are captured from air flowing around the outside of the array during flick downstrokes, when aesthetascs face upstream and molecule capture rates are 21% higher than for stationary antennules. Bursts of flicking followed by pauses deliver discrete odour samples to olfactory sensors, causing intermittency in odour capture by a different mechanism than aquatic crustaceans use.

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Transition from marine to terrestrial ecologies: Changes in olfactory and tritocerebral neuropils in land-living isopods

Cited by 35 publications

References 82 publications

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

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

Comparative analysis of deutocerebral neuropils in Chilopoda (Myriapoda): implications for the evolution of the arthropod olfactory system and support for the Mandibulata concept

Do terrestrial hermit crabs sniff? Air flow and odorant capture by flicking antennules

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