An analysis of the structure and use of the Eimers organs of the Star-nosed Mole, Condylura cristata

Rebecca Sovoda Comparative Anatomy of Vertebrates, University of Michigan-Dearborn, 2011

Abstract: The Star-nosed Mole, Condylura cristata, is a Talpid with 22 fleshy appendages circling its nostrils which are covered in Eimers organs. The nostril rays are used for the sense of touch and ingestion. Since there has been such unusual selection for these appendages, this novelty is important to observe in order to get a clear understanding of adaptation. Observing the brains relationship to the rays can explain the moles efficiency in eating, a good indicator of why the specialization was formed. I will discuss the embryonic development of the mole to observe derived characteristics. In hope of observing more details of how this adaptation occurred, I will go over the phylogeny, including how the Star-nosed mole relates to other Talpids and how the family relates to Insectivora. From an evolutionary perspective, this paper will explain the importance of Condylura cristata in understanding how specializations are brought about through natural selection for the muddy environment.
Keywords: Eimers organ, Condylura cristata, Star-nosed Mole, Talpid, Brain, Evolution, Specialization

Introduction
Condylura cristata is a unique Talpid. As a Talpid, or mole, its eyesight is diminished due to its subterranean habitat. Underground, reliance on touch is incredibly important. Through evolution, all moles have acquired tiny swellings on their noses called Eimers organs which provide an advantage in their habitat by aiding in tactile stimulation. The Star-nosed Mole has 22 1

finger-like appendages protruding from its nose (Fig 1a) where these Eimers organs can be found. The mole uses its nose in a sweeping motion as the Eimers organs (Fig 1b) feel for and distinguish prey from dirt or mud (Catania 1995b). The Star-nosed Mole has an extremely high metabolic rate, so they have acquired these appendages in order to obtain food quickly (Catania and Remple 2005). The speed of ingestion is assisted by the use of the 11th pair of rays, which help to guide food to the mouth (Catania and Kaas 1997). As fossorial animals, the family of moles (Talpidae) has acquired Eimers organs through natural selection. This provides them a more sensitive tactile ability for use in their dark underground habitat. The Star-nosed Mole has acquired its multiple appendages through natural selection due to its environment. The Star-nosed Mole is an incredible animal that has a unique adaptation for its semiaquatic environment. Looking at specific features of the Star-nosed Mole will help to provide a more thorough understanding of how evolution occurs in all species. Looking at the anatomy of the Eimers organ, the rays interaction with the brain, and also at the moles successful feeding strategy will show how the formed specialization created a great advantage for the species. Analyzing the embryology and phylogeny of the Star-nosed Mole will provide insight on how the evolution occurred in relation to its habitat. Future research of comparative anatomy will hopefully provide more details of how adaptation due to natural selection occurred in many other odd cases, like that of the Star-nosed Mole.

Relatives
Families: Looking at the closest relatives of the Star-nosed Mole gives a comparative picture of its anatomy and physiology (Symonds 2005, Sanchez-Villagra 2006). The Star-nosed Mole belongs to class Insectivora, which is very large and diverse. Symonds (2005) addressed how there are

virtually no derived morphological characteristics which made it difficult to define the families and find the true relatedness. Knowing how families are related is important in the field of comparative biology. The phylogeny illustrates the relatedness of true moles, including their derived characteristics. Talpidae are ultimately defined and set apart from other families by a synapomorphy, which is the presence of Eimers organs (Symonds 2005). In the future, a complete phylogeny of the family including the species of Talpidae would be very helpful in clarifying the divergence in characteristics leading to this specific derived trait. In the case of true moles, it is clear that the formation of Eimers organs was extremely beneficial in adaptation to their environment. In addition to morphology, DNA is another great way to add to the knowledge of phylogenetic relationships of the relatives of Talpids (Shinohara et. al. 2002). The DNA evidence helps to clarify the differences in the class Insectivora in order to create the most accurate phylogeny possible. Symonds (2005) has compiled many versions of the phylogeny in order to urge the importance of a correct phylogeny. In order to have a comparative view of a family, it is essential to know how a species differs from its closest relatives. With a complete phylogeny, Symonds (2005) argued that it would then be possible to map certain characteristics in association with selective factors. The phylogentic tree derived from DNA information shows that all true moles have Eimers organs as a result of natural selection for their environment. Sanchez-Villagra (2006) observed morphological traits to clarify derived characteristics in the phylogeny of moles. He found discrepancies which he felt were significant enough to rearrange the family Talpidae. In this research he provided evidence that the characteristic fossorial lifestyle of some shrew moles were acquired independently from Talpidae, proving that the two are not closely related. In addition, Shinohara et. al. (2002) noted that the habitat in

which many of the relatives of moles live does suggest a correlation to their phylogeny. Therefore, the habitat in which the species lives in selects for traits that would be most beneficial, causing evolution. With a more complete phylogeny it would be possible to see which characteristics evolved, including an estimated time line to see the progression of traits that led to the current distinct families.

Species: The Star-nosed Mole is the only mole to have fleshy appendages on its nose, but it is not unique in having Eimers organs. Catania (1995a), looked at three different moles, the Hairytailed Mole, the Eastern Mole, and the Star-nosed Mole and observed the physical appearances of their noses. The Hairy-tailed Mole along with the Star-nosed Mole both have visible Eimers organs all over their noses. Thin layers of keratinized skin cover the noses of all of the moles (See fig. 2). On the other hand, the organs on the Eastern Mole were not visible at all; this was due to the thick layer of keratinized skin, 40m thick (in comparison to 8 m an d16 m in the Hairy and Star-Nosed Mole respectively) (Catania 1995a). After looking at the phylogeny, the more aquatic Star-nosed Mole has diverged separately from both the Eastern Mole and the Hairy-tailed Mole because of its different environment (Shinohara et. al. 2002).

Specializations of the Star-nosed Mole

The star nose of Condylura cristata is unlike that of any other member of its family. To get a better idea of how the Star-nosed Moles nose evolved, Catania et. al (1999) analyzed embryonic development. Embryology gives a good sense of what ancestors of the Star-nosed Mole may have looked like during the process of evolution leading to its modern state. Looking

at certain stages of development, the individual rays are differentiated very early. A delicate embryonic process can be seen in the formation of the rays. This process occurs when deep layers of the epidermis grow and cause the surface of the epidermis to buckle. When the embryo of the Star-nosed Mole was about 11mm long, the first sign of the star was noticed as a fold. As the folding continued during the embryonic development, the star nose became more pronounced. Primitive adult Star-nosed Moles would have looked similar to current-day embryos, with small folds. As an adult, the individuals were better suited to the extremely moist, subterranean climate. Due to natural selection for a larger nose, the moles with longer folds reproduced in greater numbers. Through the next generations, the star nose became more specialized for its environment and the rays became more distinct. The current star nose is now modified to 22 unique appendages that prove to be extremely useful (Catania et. al. 1999).

Eimers Organ Anatomy

The structure of an individual Eimers organ is very complex (Fig. 2). Each papillae is made of epidermal cells that are stacked on top of each other (Catania 1996). A swelling forms at the top of the epidermis where all the nerve fibers come together and gives the organ its shape. The epidermis is thin, and is composed of the stratum corneum (Catania 1996), and a thin layer of keratinized cells (Catania 1995a). In addition, a nerve terminal runs through the center of the cell and into the terminal cell, known as the central disk. The central disk has satellite processes surrounding it to aid in the neural pathway. A Merkel cell sits at the bottom of the organ to receive sensory input, an important function for all Talpids (Catania 1995b). Below the Merkel cell, there is an encapsulated corpuscle, which is a mass that holds the nerve ending on the receptive end (Marasco et. al 2006).

From looking at the anatomy of an individual Eimers organ, it is clear that each ray is an extension of the epidermis. The swelling is caused as the nerve fibers run to the surface of the skin (Catania 1995a). At the surface, the swelling can come into contact with its prey through the epidermis. Due to the environment that Condylura cristata lives in, Catania (1995a) found that they have acquired smaller and more numerous sensory organs in comparison to other Talpids. In addition, the 22 long extensions were extremely useful in muddy terrain. Both of these features have leaded the mole to be incredibly sensitive to the touch.

Brain
The nasal appendage of the Star-nosed Mole has special innervations in the brain (Catania and Kaas 1995b). Since the eyesight and hearing of the mole are diminished, an increasing amount of the surface area of the brain that is dedicated to the sense of touch. Due to the large number of nerves, there is a very strong representation of the nose over other parts in its cortical innervations. This change in the brain causes a magnification of tactile stimulation in the cortex (Catania and Kaas 1995b). When analyzing the representation of the star and the rest of the body, researchers were able to map these innervations in the brain. Facial sensation such as the whiskers, mouth, and rays are located in a lateral ventral region of the brain. Catania and Kaas (1995) observed the brain as objects were put into contact with the individual rays. The researchers were able to identify which areas of the cortex were stimulated by a particular ray. Catania and Kaas (1995) noticed while mapping the brain, that similar to humans, there is a contralateral correlation represented in the brain in numerical order corresponding to the 11 rays. Catania and Kaas (1996 and 1997) explained how the physical proportions of the Starnosed Mole relate to the cortical representation. By touching different areas of the body, the

researchers were able to map these body parts to the different areas of the brain that they innervate. In cases of specialization, it is clear that there is a magnification which shows a higher sensitivity or more of a use for the particular body part. In comparison to its digits, for the sense of touch, the specialized Eimers organ had a much stronger cortical representation in the brain (Catania and Kaas 1996; Catania 2005). When eating, Condylura cristata, uses the 11th set of rays to aid in ingestion by helping to guide food to the mouth (Catania and Kaas 1997). This 11th set of rays happens to be the most used rays, which is why the magnification in the brain was observed to be greater than that of the other rays. In addition to cortical representation in the brain, the superior colliculus is a portion of the brain that works with eyesight (Crish et al. 2003). Since eyesight is not heavily relied upon in the Star-nosed Mole, this area of the brain is not diminished but rather it has been converted to relay tactical stimulation as a visual sense to the mole (Crish et al. 2003). Not only do the rays correspond to the area of the cortex that functions with motor and sensory, but also innervates superior colliculus, and in theory a sense that is felt visually. This may be an additional reason why the star-nose is so sensitive.

Feeding
The anatomy of the Star-nosed Mole is largely a function of its eating habits. The Starnosed Mole supplements its diet with a variety of organisms such as night crawlers and crayfish (Catania and Kaas 1997). Morphologically, characteristics of the closest relatives of the Starnosed Mole are very similar in body shape and size, but what separates this species from the next are their unique facial features (Catania, K. C. 1995a). The star nose has made the snout elongated and bony. The masticator muscles are not as strong as some of the other species in its

family. The cartilaginous part of its mouth is at a different angle compared to its closest relatives (Grand et al. 1998). This makes the overall structure of the snout of the Star-nosed Mole fragile (Grand et al. 1998). Although its jaw tends to be weak, this feature happens to be a trade-off for the species. Since the masticator muscles are not built strong enough to eat large food, their specialization, the Eimers organ, allows the mole to be more selective. Catania and Remple (2005) used an equation to determine how successful the Star-nosed Mole is in finding food. This in turn gives mathematical data which would represent how advantageous the star nose is in eating. This research concluded that the speed at which Starnosed Mole ate was extremely fast. This enabled the mole to eat smaller prey such as extremely small earthworms or invertebrates and still manage to maintain the high demands of its metabolic rate (Catania and Remple 2005). (See info box 1). Therefore, since the rate of ingestion is so high, the quality of the food (E) can be lower and still get a good rate of energy intake (R).

Conclusion
Overall, the structure of the Star-nosed Mole is extremely unique. Although general characteristics can easily be compared to other Talpids such as diminished eye sight, and reliance upon somatosensory stimulation through the Eimers organs, the Star-nosed Mole has acquired its own special characteristics. The 22 appendages are heavily covered in Eimers organs, which allow for highly sensitive touch reception. DNA evidence which aided in the creation of a phylogeny and embryonic development showed how the evolution of the star came about. The phylogeny showed derived characteristics. This is very important in the field of comparative anatomy in order to see how the species formed the specific traits, and then determine if they correlate with any other aspect of life that would cause this adaptation. In the case of the Star-

nosed Mole, this happened to do with the muddy and semi-aquatic terrain. The embryology of the Star-nosed mole showed how its ancestors may have looked through evolution. The more primitive Star-nosed Moles had a nose which showed signs of the formation of the distinct rays. In the following generations, the enlarged nose became advantageous in its habitat and eventually the star nose was derived. The Star-nosed Moles rays have an extremely fast reaction time allowing it find and ingest a large quantity of food essential to meet the needs of its high metabolic rate. This usefulness of the rays are another function of adaptation to the wet environment. To innervate the complex ray system, the brain must represent the usage of the rays cortically, in addition the use of the rays is observed in the superior colliclious which is usually used for sight. Through research of the Eimers organ and the study of behavioral traits of the Star-nosed Mole showed that the moles unique snout is essential for the survival of the species in its specific habitat. The study of adaptation is incredibly specific to an individual species particular case. For the Star-nosed Mole, several questions are still present surrounding the workings of the star nose. The complex brain allows for this astounding sensitivity of the nose. Researchers were able to obtain great data in the area of anatomy, but in terms of physiology, further research could help explain how the sensitivity works. In particular, the specialization of the superior colliculus, which in most species works with eyesight, is converted to relay tactical stimulation. How this works is still not completely understood. This includes how the mole perceives this sensation. Working in the field of comparative anatomy, future research could provide solutions to many of the holes in phylogeny of Talpidae. Studying how other species have adapted to their environment can help explain the workings of the phylogeny, just as in the case of the Star-nosed Mole. Adaptation is a universal concept which holds true in all habitats and in all species. This

research paper gave a good summary of how this process happend in the Star-nosed Mole. By studying the phylogeny of other species such as one of my favorites, the Proboscis Monkey, more can be learned in this ever changing field. By observing the phylogeny of some unusual animals such as this one, it would be easier to understand how the evolution of the monkeys huge nose came about through selective forces. In addition, this would give a better understanding of how adaptation occurs and possibly predict evolutionary change due to selective forces for other species.

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Glossary:
Contralateral-affecting the other side (Catania and Kaas 1995). Eimers organ- the structure on the snout of moles which provide and relay tactile information to the brain through the use of the somatosensory system (Catania, K. C. 1995a, 1995b, 1996). Fossorial- an animal adapted for burrowing and living underground (Catania 1995b). Papillae- bump, projection or elevation (Catania 1996). Somatosensory- sensations from skin/tissues (Catania 2005). Superior colliculus- structure in the brain that receives sensory imput (Crish et al. 2003). Talpids- family Talpidae, the moles (Sanchez-Villagra, M. R. Horovitz, and I. Motokawa, M. 2005).

Box 1: R= E + Th Ts

R=rate of energy intake E= energy obtained from prey Ts= Time spent searching Th= Time spent handling prey Since Ts and Th are both inversely proportional to R, if the time spent searching and the time spent handling the prey are both minimized, the rate of energy intake would increase. Since the energy from a particular food source is dependent upon the quality of the food, as its speed is increased, both in searching and in handling, the rate of energy intake in the Starnosed Mole is increased (Catania and Remple 2005)

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Figures:

Figure 1a. The nose and appendages of the Starnosed mole. The individual rays are labeled 1-11 then 12-22 on the other side. The 11th set of rays are shorter and aid in ingestion Figure 1b. Picture of an individual ray covered in Eimers organs.

Figure 2. A cross-section of an Eimers organ. The superficial layer of skin is the epidermis and a thin layer of keratinized skin cells on top. The dermis, the lower level, contains all of the internal structures. The central disk has a nerve running through it and the satellite processes that aid in the pathway. The merkel cell receives sensory input and the encapsulated corpuscle holds the nerve endings.

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References:
Catania, K. C. (1995a). A comparison of the Eimer's organs of three North American Moles: The Hairy-tailed Mole (Parascalops breweri), the Star-nosed Mole (Condylura cristata), and the Eastern Mole (Scalopus aquaticus). The Journal of Comparative Neurology, 354: 150160. Catania, K. C. (1995b). Structure and innervation of the sensory organs on the snout of the Starnosed Mole. The Journal of Comparative Neurology, 351: 536548. Catania, K. C. (1996). Ultrastructure of the Eimer's organ of the Star-nosed Mole. The Journal of Comparative Neurology, 365: 343354. Catania, K. C. (2005). Evolution of sensory specializations in insectivores. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology, 287A: 1038 1050. Catania, K. C. and Kaas, J. H. (1995). Organization of the somatosensory cortex of the Starnosed Mole. The Journal of Comparative Neurology, 351: 549567. Catania, K.C. and Kaas, J. H. (1996). The unusual nose and brain of the Star-nosed Mole:A star in the brain. Bioscience, 46: 578. Catania, K. C. and Kaas, J. H. (1997). Somatosensory fovea in the Star-nosed Mole: Behavioral use of the star in relation to innervation patterns and cortical representation. The Journal of Comparative Neurology, 387: 215233. Catania, K. C. Northcutt, R. G. and Kaas, J. H. (1999). The development of a biological novelty: A different way to make appendages as revealed in the snout of the Star-Nosed Mole Condylura cristata. The Journal of Experimental Biology 202: 27192726. Catania, K. C. and Remple, F. E. (2005). Asymptotic prey profitability drives star-nosed mole to the foraging speed limit. Nature, 433: 519.

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Crish, S. D. Comer, C. M. Marasco, P. D. and Catania, K.C. (2003). Somatosensation in the superior colliculus of the Star-nosed Mole. Journal of Comparative Neurology, 464: 415425. Grand, T. Gould, E. and Montali, R. (1998). Structure of the proboscis and rays of the Star-nosed Mole, Condylura cristata. Journal of Mammalogy, 79: 492-501. Marasco, P. D. Tsuruda, P. R. Bautista, D. M. Julius, D. and Catania, K. C. (2006). Neuroanatomical evidence for segregation of nerve fibers conveying light touch and pain sensation in Eimers organ of the mole. PubMed Central, 103: 9339-9334. Sanchez-Villagra, M. R. Horovitz, and I. Motokawa, M. (2005). A comprehensive morphological analysis of talpid moles phylogenetic relationships. Cladistics, 22: 59-88. Shinohara, A. Campbell, K. L. and Suzuki, H. (2002). Molecular phylogenetic relationships of moles, shrew moles, and desmans from the new and old worlds. Molecular Phylogenetics and Evolution, 27: 247-258. Symonds, M. R. E. (2005). Phylogeny and life histories of the Insectivora: Controversies and consequences. Biological Reviews, 80: 93128.

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