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The Size of Major Mammalian Sensory Organs as Measured from Cranial Characters, and Their Relation to the Biology and Evolution of Mammals

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Title: The Size of Major Mammalian Sensory Organs as Measured from Cranial Characters, and Their Relation to the Biology and Evolution of Mammals
Author: Pihlström, Henry
Contributor: University of Helsinki, Faculty of Biological and Environmental Sciences, Department of Biosciences, Fysiologi och neurovetenskap
Thesis level: Doctoral dissertation (article-based)
Abstract: The basic functional principles of the major sensory systems of mammals (e.g., vision, hearing and olfaction) are fairly well understood. Within certain limits, increasing the size of the structures that collect the adequate physical signals and transduce them into neural responses is a priori expected to improve sensory performance, and the relative size of a sensory organ might provide a simple measure of the relative importance of the corresponding sense. If investments into complex sensory organs can be expressed by simple anatomical measures, this would facilitate large-scale comparative studies of the ecology and evolutionary history of the sensory modalities in different groups. Although sensory organs mainly consist of soft tissues, they are embedded in bony structures and some include functional bony components. Thus it is possible to define potentially relevant osteological dimensions that can be measured from both extant and extinct (fossil) species, and this is the point of departure of the present thesis.

The original measurements focus on two senses, olfaction and vision. In the first study, the area of the cribriform plate of the ethmoid bone is defined, measured, and validated as a useful hard-tissue anatomical proxy for the sensitivity of olfaction in various mammalian groups. It is shown that cribriform plate area (representing olfactory organ size) grows proportionally to skull area (representing animal size), with no sign of levelling off in the highest range. There are only a few taxa that have smaller olfactory organs than expected : these include monkeys and apes on the one hand, and the aquatic dugong on the other. The semi-aquatic pinnipeds, by contrast, have cribriform plate areas comparable in size to those of similar-sized terrestrial carnivores.

In the second study, the analysis of orbit size as a proxy for eye size, which has previously been used for primates by several authors, is applied to a comprehensive mammalian data base of 355 species representing most major orders, largely based on new original measurements. It was first shown that the eyes of the groups included are effectively spherical and that the relation between eye and orbit size is regular enough for the orbit to be informative of eye size and thus visual sensitivity/acuity. The earlier primate studies have found that (small) nocturnally active species have relatively larger orbit diameters than diurnally active species of similar size. While this was confirmed for primates, no general diurnal/nocturnal difference in orbit size at the same skull size was found in non-primate mammals. The allometric growth of orbit size with increasing skull size was steeper for nocturnal than diurnal mammals, but the significance of this is unclear, as the former sample was dominated by smaller species compared with the latter sample. In cathemeral species (i.e., species active during both night and day), the allometric relation of orbit size to skull size was more similar to that of nocturnal than of diurnal species. Taken together, the results suggest that relative orbit diameter is not a useful indicator of the diel activity pattern of non-primate mammals, and cannot be used to infer the pattern of fossil species.

In the third study, the question of the trade-off relations between three major senses, vision, hearing, and olfaction, was investigated. The proxy measure used for the auditory organ was the size of the middle ear bones as reported by Nummela et al. (1995). The residual size of each organ in each species was calculated as its deviation from the global mammalian regression line relating the respective organ proxy size to body size. The residuals were plotted into a three-dimensional sensory space , where the coordinate axes represent vision, hearing, and smell. This provides a graphic representation of correlations between organ sizes, both positive and negative. The results suggested that good vision and hearing are often positively correlated in mammals; thus, it seems that investments in eyes and ears are likely to co-operate rather than compete. By contrast, it appeared that a keen sense of smell rarely occurs together with equally keen vision and/or hearing.I denna avhandling visar jag hur man genom skallmätningar kan undersöka nu levande däggdjurs sinnesorgan och deras relativa betydelse för livsföringen hos diverse olika arter. För att kunna kvantitativt undersöka de olika sinnesorganen har jag mätt utvalda anatomiska delar av däggdjurs skallar. De sinnesorgan som jag i första hand har undersökt är doft- och synsinnet. Som mått på doftsinnet har jag använt det så kallade silbenets yta i förhållande till själva skallens yta, och som mått på synsinnet har jag använt ögonhålans diameter i förhållande till skallens längd. För att kunna använda dessa respektive skelettstrukturer som mått på sinnesorganens skärpa är det först nödvändigt att påvisa att dessa strukturers storlek verkligen hänger funktionellt sett direkt ihop med de relevanta mjukvävnadsstrukturerna. Jag påvisar i min avhandling att silbenets yta korrelerar direkt med doftepitelets yta (som i sin tur funktionellt hänger ihop med doftskärpan), och att ögonhålans diameter korrelerar direkt med själva ögats storlek (som i sin tur funktionellt hänger ihop med synskärpa och -känslighet). Med andra ord, genom att mäta silbenets eller ögonhålans storlek i förhållande till skallens storlek hos ett givet däggdjur kan man säga hur pass väl utvecklade dessa respektive sinnen är hos den.

Mina resultat visar att silbenets yta inte varierar med kroppsstorlek: små däggdjur har relativt sett lika stora silbensytor som stora däggdjur. De mest avvikande däggdjuren beträffande silbenets yta/doftsinnets storlek är dels de mest strikt vattenlevande arterna, dels aporna och människan; dessa däggdjur har relativt sett betydligt mindre silbensytor (och i vissa fall till och med funktionellt fullständigt förkrympta sådana) än övriga däggdjur, vilket tyder på att de har ett relativt svagt utvecklat doftsinne.

Beträffande ögonhålans relativa storlek hos däggdjur har jag jämfört denna mellan dags- och nattaktiva arter; dylika undersökningar har tidigare utförts på primater, men inte i någon större skala på övriga däggdjur. Mina mätningsresultat visar att till skillnad från primater, bland vilka nattaktiva arter har relativt sett tydligt större ögonhålor än dagaktiva arter, uppvisar övriga däggdjur inga tydliga skillnader mellan dag- och nattaktiva arter. Detta betyder att ögonhålans storlek inte kan användas för att rekonstruera levnadssättet hos utdöda, fossila icke-primater.

Slutligen har jag också undersökt hur och på vilket sett doft-, syn- och hörselsinnet samarbetar med eller ersätter varandra (som mått på hörselsinnet använder jag hörselbenens relativa storlek). Resultaten tyder på att god syn och god hörsel ofta hänger ihop hos däggdjur, medan däremot en art som har ett stort doftorgan sällan har särskilt stora ögon eller stora hörselben. Med andra ord, det tycks råda en viss "arbetsfördelning" mellan dessa tre sinnen.
URI: URN:ISBN:978-952-10-8557-4
http://hdl.handle.net/10138/37713
Date: 2012-12-15
Copyright information: This publication is copyrighted. You may download, display and print it for Your own personal use. Commercial use is prohibited.
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