Source: UNIVERSITY OF NEBRASKA submitted to
EVOLUTION, BIOMECHANICS, AND FUNCTION IN THE TEETH, JAWS, AND SKULLS OF INSECTIVOROUS MAMMALS
Sponsoring Institution
State Agricultural Experiment Station
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
0203769
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
May 1, 2005
Project End Date
Apr 30, 2010
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIVERSITY OF NEBRASKA
(N/A)
LINCOLN,NE 68583
Performing Department
SCHOOL OF NATURAL RESOURCES
Non Technical Summary
The progression of the primitive tooth form in insect-eating mammals can be traced to more derived forms that eat fruit, meat, and nectar. This is an investigation to examinie exactly how insectivore teeth interact with foods eaten and involves understanding how hard and soft-shelled insects are being processed. This is an area of basic dental research of the most primitive food habit in mammals and is a rich area of research because the texture and nature of foods dictates tooth shape over time. Biomaterials such as insects and how they are processed by teeth is not well understood. Dental trends from primitive (insectivory) to derived food habits (frugivory and omnivory) are relevant to many mammals including primates and with greater understanding could influence the nature of foods available to mammals including humans.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
13508301070100%
Knowledge Area
135 - Aquatic and Terrestrial Wildlife;

Subject Of Investigation
0830 - Wild animals;

Field Of Science
1070 - Ecology;
Goals / Objectives
Understanding and quantifying what is happening at the tooth/food interface of insectivore and prey is basic knowledge that will help us understand more about how teeth work and how they have evolved to accommodate different diets in mammals. More than in any vertebrate group, the teeth of mammals are a window to their diets and this relationship is not trivial. Not only is tooth shape closely related to diet, it is also the subtle differences in shape of the teeth and cusps that often determine different species in mammals. Further, because teeth are a hard material, they fossilize well and are often the only evidence of the identification and the biology of ancient mammals.
Project Methods
My research has centered on extensive and detailed study of the morphology of bat teeth, jaws, and skulls. I use three approaches. The first is to describe and quantify the shapes of the skulls, jaws, and teeth of bats and to make predictions as to what the animal is doing ecologically. These predictions are supported by both my data and evidence from the literature. Bats have a single ancestor and are therefore more closely related to other bats than to any other group of mammals. Living bats have an unusual diversity in food habits that is reflected in specific morphological signatures in their jaws, skulls, and teeth. I have been able to use these signatures to trace how insectivory changes into nectarivory, frugivory, and carnivory. The second level is to test my predictions experimentally. I have begun experimentally testing the toughness of insect cuticle and the corresponding strength of canine teeth that have different cross-sectional shapes. Establishing the forces it takes to cut a diversity of insect prey known to be eaten by bats will not only pioneer a new area of materials science, it will also verify predictions that have long been used in the literature. Tooth strength and shape may be well known for humans, but few data are available for most mammals. Quantifying tooth strength and insect prey are prerequisites to understanding what occurs at the tooth/food interface. The third level is to investigate ways of analyzing skull shape changes, the evolution of skull shape, and the evolution of different skull shapes among families of mammals. Quantifying the adaptive radiation in Chiroptera and particularly Microchiroptera has produced rich insight and understanding of the evolution in a monophyletic group. This approach can be just as rich for explaining the evolution in different groups of modern terrestrial insectivorous mammals.

Progress 05/01/05 to 04/30/10

Outputs
OUTPUTS: From this project there have10 peer-reviewed papers including one invention, one applied publications, and one grant proposal. I have experimentally tested what shapes of idealized canine teeth are best for puncturing different biological materials. Canines with triangular cross-sections are best for puncturing insects. I have discovered new fundamental knowledge about mammaliandentin. After experimentally breaking canine teeth of several mid-sized carnivores, I found that coyotes have stronger dentine than that in humans. After developing the protocol, I was able to collect and cut local insects with specialized equipment and measure the forces necessary to separate the insect. Moths are significantly softer than beetles of the same size. My co-author and I invented a significant new device to measure the force necessary for small rodents and bats to bite. It is a piezo-electric sensor for use in the field while the living animal is fresh. Knowing these forces are an important step in knowing whether certain mammalian insect predators can consume a certain hardness of insect, which we have also measured. We have published bite forces in commonly caught rodents in Nebraska and correlated that information with different morphological indices of bite forces in rodents and have been able to recommend which index most closely estimates the actual bite force measured by the sensor. In a more applied project I was able to use bat and rodent bite force data to test the which leather gloves provide field biologists and students the best protection as he/she is handling small mammals, particularly bats that are delicate and easily tangled in nets. Leather gloves are best to use for protection against small, medium and large-sized bats. Deer skin is unusually resistant to puncture and gives more dexterity for its thickness. This paper was published in the Journal of Wildlife Management and singled out as a field technique of interest in JWM's sister publication, The Wildlife Professional (Field Notes: Tough Glove. Spring 2010: 72) From this research I submitted a proposal to the National Science Foundation in 2009 to continue to work in the tropics with undergraduate students. This was not funded. However, a byproduct of my research resulted in a publication on the biodiversity and reproduction of bats in Trinidad during the dry season, a time when few studies have been done. Finally, bite forces of bats in Nebraska, New Mexico, Utah, Texas, Trinidad and Tobago were regressed against several different morphological indices of bite forces in bats. Our model derived from beam theory relies on bony characteristics, which are readily available from museum specimens. This model will be of particular use to students of fossils or ecomorphology for inferring bite force. This publication in the Journal of Zoology was singled out as a paper of interest for the last quarter of 2010 and for interview with a podcast which is or soon will be online (http://www.wiley.com/bw/podcast/jzo.asp). PARTICIPANTS: Dr. Cliff Lemen earned his PhD at the University of New Mexico in 1977 and is a mammalian ecologist and evolutionary biologist. We continue a close collaboration in all of this research. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
Most biomechanics of teeth is done on humans or domesticated mammals. I am pioneering this area for wild mammals and am finding significant differences. I can now build a much more credible model of how strong canine teeth need to be for particular diets and in fossil or rare mammals. We quantified rate of taper in the canine tooth in several species of felids, and by assuming this was the optimal design we determined the relative costs of breakage and puncturing that would produce such a taper. Then we used the relative costs to predict the aspect ratio of the optimum tooth. The average predicted value is very close to the average value in extant species of cats. We think we can now predict the best shape a canine tooth should be to optimize its ability in strength and ability to pierce an animal's hide, which has useful application in interpreting fossil teeth, teeth of rare animals, and possibly, how tough a material has to be to withstand being punctured by such teeth. Dentin in the coyote's canine is not homogeneous. Dentin is more ductile further away from the pulp cavity. Modulus of rupture first increases and then declines with distance from the pulp cavity. Analysis of the composite nature of dentin produced by these gradients indicates there may be an adaptive explanation with the composite having nearly the strength of the strongest dentin and a work of fracture greater that even the most ductile dentin. Coyote dentin is considerably stronger than human dentin. Enamel plays, at most, a small role in the bending strength of the whole tooth. Techniques I have pioneered for measuring forces in small mammals are being adapted for other wildlife projects. Which gloves undergraduates should use for a field Mammalogy class for netting bats has now been posted different websites by mammalogists. Much of this research has been published in the, Journal of Zoology, which recently was named as one of the 10 most influential journals in Biology and Medicine from the last 100 years by the SLA (Special Libraries Association) conference. Further, another outlet for my research, the Journal of Mammalogy has been ranked in the top 100 most influential journals in Biology and Medicine by the same organization. My publications are available for public access on the Digital Commons website of the University of Nebraska-Lincoln (http://digitalcommons.unl.edu). These entire papers have now been downloaded about 3000 times during the time period of this project.

Publications

  • Freeman, P.W., and Cliff A. Lemen. 2010. Simple predictors of bite force in bats: the good, the better and the better still. Journal of Zoology, Journal of Zoology, early-view online 19 August 2010: 1-7.


Progress 10/01/08 to 09/30/09

Outputs
OUTPUTS: I published 2 publications on this topic in 2009. I have been able to measure bite forces in commonly caught bats in Nebraska, Texas, Trinidad and Tobago and correlated that information with different morphological indices of bite forces in bats. I can now recommend which index most closely estimates the actual bite force measured by the sensor. This paper is nearly ready for publication. In addition, I submitted a proposal to the National Science Foundation to continue this work in the tropics with undergraduate students. I successfully published a paper in the Journal of Wildlife Management recommending which leather gloves are best to use for protection against small, medium and large-sized bats. They were all tough gloves, but deer skin is unusually resistant to puncture and gives more dexterity for its thickness. Further, because of the success of my work in Trinidad and Tobago, my colleagues and I have published a paper on biodiversity and reproduction of bats in Trinidad during the dry season, a time when few studies have been done. PARTICIPANTS: Patricia Freeman is PI of this project and the prime mover of this research. She and her co-PI captured and fed different species of local bats and began to test which insects are harder and more difficult to chew. She also lead 2 field trips to Big Bend National Park one with students and one with her co-PI. Important species and data were collected and used in a proposal she wrote for the National Science foundation. A paper is nearly completed summarizing her data an bite forces in bats. Cliff Lemen is co-PI on this project. He is a PhD biologists and without his expertise and experience, Freeman could not have accomplished what she has accomplished. Collaborators, Keith Geluso and Mary Harner, assistant professors at University of Nebraska at Kearney have assisted Freeman and Lemen in the past in Trinidad and will be involved if funding is available for further tropical work. Keith Geluso is an expert field biology with much experience in the tropics. TARGET AUDIENCES: Freeman's research is basic biological research and targeted at whole organism scientists and students. With funding there is a possibility of collaboration with an pest insect scientist at the University of the West Indies in Trinidad. Efforts at spreading my research primarily take the form of showing students in my classes how my techniques are used with wild bats in the field and what the research can tell us about bats and their prey. Further, upper level high school students and early university students have been written into a moderately large proposal to NSF so that I can take them and Trinidadian students to the field in Trinidad. There I hope to show them the biodiversity of tropical bats and insects and have them help me collect data for this project. This past spring I and 2 other faculty took a class to Big Bend National Park and netted bats for this project. Numbers were low but it was a successful trip. PROJECT MODIFICATIONS: The original project involved fabricating teeth and using them in tests to quantify how they are used in chewing. The current direction of project is more focused on using live materials and measuring toughness of insect prey. My co-PI and I are now confident that we can raise bats in captivity and provide a variety of common foods that vary in how hard they are to chew. Should funding become available we will increase the number of species used and the variety of prey to be eaten.

Impacts
The above papers have been published in well-established journals. The Journal of Wildlife Management is a premier journal for wildlife publications. Because my papers are posted on the university's digital common website (http://digitalcommons.unl.edu) I know that the last 9 papers, ones most concerned with this project have been downloaded 1,893 times for an average of 210.3 downloads per paper. Further, the techniques I have pioneered for measuring forces in small mammals are being adapted for other wildlife projects. Which gloves undergraduates should use for a field Mammalogy class for netting bats has now been posted different websites by mammalogists.

Publications

  • Freeman, P.W., and Cliff A. Lemen. 2009. Puncture-resistance of leather gloves for handling bats. Journal of Wildlife Management, 73: 1251-1254.
  • Geluso, K, M.J. Harner, C.A. Lemen, and P.W. Freeman. 2009. Survey of bats in northern Trinidad late in the rainy season. Occasional Papers of the Museum of Texas Tech University, 285: 1-13.


Progress 10/01/07 to 09/30/08

Outputs
OUTPUTS: I have produced three publications on this topic in 2008. For the time being we are moving away from tooth breaking experiments in midsized carnivores with our most recent paper on that topic in the Journal of Zoology to other topics. The description of our invention of a small sensor to measure bite force in small mammals has been published. It has opened numerous exciting paths of investigation. We have been able to measure bite forces in commonly caught rodents in Nebraska and correlated that information with different morphological indices of bite forces in rodents and have been able to recommend which index most closely estimates the actual bite force measured by the sensor. This paper came out in the Journal of Zoology. Data collection on bite forces of bats from mesic and xeric habitats has been collected and is being analyzed. The diversity of bats from Trinidad and Tobago have greatly increased the breadth of species. Another project has been to use the bat and rodent bite force data to test the protection that different leather gloves may give the field biologist as he/she is handling small mammals, particularly bats that are delicate and easily tangled in nets. PARTICIPANTS: Dr. Cliff Lemen, Adjunct Professor, School of Natural Resources and University of Nebraska State Museum, and I do all field and lab work together. He is a skilled biologist, ecologist, mammalogist, ornithologist, mathematician, computer expert, machinist, and electronics inventor. Dr. Keith Geluso, Assistant Professor, University of Nebraska-Kearney, is an excellent and knowledgeable biologist who accompanied us to Trinidad and Tobago. In the course of collecting data we also surveyed the bats on these two islands. TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
The above papers have been published in well-established journals. The Journal of Mammalogy goes to nearly 4,000 members in all 50 of the US and 60 other countries worldwide. The Journal of Zoology is similar. Because my papers are posted on the university's digital common website (http://digitalcommons.unl.edu) I know that the last 6 papers, ones most concerned with biomechanics of mammal teeth, are being downloaded at a rate of 22 per month. The rate for all of my papers being downloaded in the past 30 months has been 264 per month.

Publications

  • Freeman, P.W., and Lemen, C.A. 2008. A simple morphological predictor of bite force in rodents. J. Zool. (London) 275: 418-422.


Progress 10/01/06 to 09/30/07

Outputs
OUTPUTS: Activities have involved conducting field work in trapping mammals, netting bats and lab/computer work in breaking experiments with dentin from the teeth of coyotes and formulating finite-elements analysis of teeth. More that thirty days of field work were conducted in Nebraska, New Mexico, and Utah. New fundamental knowledge was gathered about coyote and human dentin. Further, my co-author and I invented a significant new device to measure the force necessary for small rodents and bats to bite. It is a piezo-electric sensor for use in the field while the living animal is fresh. The applied aspects of this bite-force sensor are being explored, but it has improved the knowledge we currently have on mammalian bite forces. Knowing these forces are an important step in knowing whether certain mammalian insect predators can consume a certain hardness of insect, which we have also measured. Dissemination of my research has been primarily through publication of in scientific journals. In 2006 Journal of Zoology was circulated to 3519 institutions worldwide. In terms of readership, JZO received 63,667 downloads (papers accessed via the web)in 2006. It is impossible to know how many readers use the printed hard copy. However, I have placed all my published papers for public access on the Digital Commons website of the University of Nebraska-Lincoln (http://digitalcommons.unl.edu). In the past 19 months my papers (52) have been downloaded 5,015 times for an average of 264 downloads/month. My last paper of 2006 and the first 2 of 2007 are averaging 22 downloads/month. PROJECT MODIFICATIONS: My research has veered a bit off target in that I have moved away from fabricating teeth in the lab to actually testing living animals in the field. I am also dissecting and weighting jaw muscles of the mammals in question whether they are insectivorous bats or omnivorous rodents. The invention of our bite-force sensor has really opened the arena up and I am pursuing that aspect.

Impacts
We quantified rate of taper in the canine tooth in several species of felids, and by assuming this was the optimal design we determined the relative costs of breakage and puncturing that would produce such a taper. Then we used the relative costs to predict the aspect ratio of the optimum tooth. The average predicted value is very close to the average value in extant species of cats. We think we can now predict the best shape a canine tooth should be to optimize its ability in strength and ability to pierce an animal's hide, which has useful application in interpreting fossil teeth, teeth of rare animals, and possibly, how tough a material has to be to withstand being punctured by such teeth. Dentin in the coyote's canine is not homogeneous. Dentin is more ductile further away from the pulp cavity. Modulus of rupture first increases and then declines with distance from the pulp cavity. Analysis of the composite nature of dentin produced by these gradients indicates there may be an adaptive explanation with the composite having nearly the strength of the strongest dentin and a work of fracture greater that even the most ductile dentin. Coyote dentin is considerably stronger than human dentin. Enamel plays, at most, a small role in the bending strength of the whole tooth. A colleague and I have invented a slim, plastic, piezo-resistive sensor for quantifying bite force in live, small mammals that is battery-operated unit and ideal for field research. We tested this sensor in the lab and in the field on a variety of small mammals. The small size and ease of use of the piezo-resistive detector is highly successful. This device will significantly improve our predictions of bite force in both living and fossil mammals.

Publications

  • Freeman, P.W., and Cliff A. Lemen. 2007. The tradeoff between strength and tooth penetration: Predicting optimal shape of canine teeth. Journal of Zoology (London), 273:273-280.
  • Freeman, P.W., and Cliff A. Lemen. 2007. An experimental approach to quantifying strength of canine teeth. Journal of Zoology (London), 271:162-169. 9 Feb.(ARD#15090)
  • Freeman, P. W., and Cliff A. Lemen. 2007. Using scissors to quantify hardness of insects: Do bats select for size or hardness? Journal of Zoology (London), 271:469-476. 20 March (ARD#15247)
  • Freeman, P.W., and Cliff A. Lemen. 2008. Material properties of coyote dentin under bending: gradients in flexibility and strength by position. Journal of Zoology (London)(in press)
  • Freeman, P.W., and Cliff A. Lemen. 2008. Measuring bite force in small mammals with a piezo-resistive sensor. Journal of Mammalogy(#2)(in press)


Progress 10/01/05 to 09/30/06

Outputs
I have experimentally tested what shapes of idealized canine teeth are best for puncturing different biological materials. Canines with triangular cross-sections are best for puncturing insects. After experimentally breaking canine teeth of several mid-sized carnivores, I found that coyotes have stronger dentine than that in humans. Strength of tooth is highly correlated with weight of animal, and I can now predict the strength necessary for an unusual animal such as a saber-toothed cat. More experimentation will have to be to be done to see where small sized mammals fit on the regression line. After developing a protocol, I was able to collect and cut local insects with specialized equipment and measure the forces necessary to separate the insect. Moths are significantly softer than beetles of the same size. Other orders of insect were also softer than beetles. Beetles have more variation in the species examined.

Impacts
I am making significant inroads into understanding the forces necessary to process prey of carnivorous and insectivorous mammals and how size and shape of canine teeth affect those forces. Most biomechanics of teeth is done on humans or domesticated mammals. I am pioneering this area for wild mammals and am finding significant differences. I can now build a much more credible model of how strong canine teeth need to be for particular diets and in fossil or rare mammals.

Publications

  • Freeman, P.W. and Lemen, C.A. 2006. Puncturing ability of idealized canine teeth: edged and non-edged shanks. Journal of Zoology (London), 269: 51-56. (ARD#14927).
  • Freeman, P. W., and C.A. Lemen. 2006. In Press. Using scissors to quantify hardness of insects: Do bats select for size or hardness? Journal of Zoology (London) (ARD#15247)
  • Freeman, P.W., and C.A. Lemen. 2006. In Press. An experimental approach to quantifying strength of canine teeth. Journal of Zoology (London) (ARD#15090)


Progress 03/01/05 to 12/31/05

Outputs
Experimentation with models of canine teeth with non-edged (circular) and edged (triangular) cross-sections shows that penetration generally takes less force for the edged tooth. However, ease of penetration can be affected by food type. In trying to understand the optimum shape of the main puncturing tooth, I have found that having an edge is an effective tool for getting into a food package. I am currently continuing this line of investigating by cutting a variety of fresh insects to quantify exactly what forces are needed to divide the insect. In trying to determine the actual strength of a single canine tooth, I have experimentally broken fresh canine teeth of carnivores and quantified the forces necessary to break the tooth. With these data I have been able to model the breaking load for not only different-sized carnivores but also for much smaller teeth. Strength of tooth and body weight of the mammals are highly correlated.

Impacts
Knowing how hard insects are to process could affect which natural predators could prey upon specific insects, including insect pests. Understanding that certain insects are predictably harder than others means that predictions can be made about different communities of insects and whether local mammalian predators that can eat them. Most importantly however is teasing out form and function of teeth at the tooth/food interface and contributing to the basic knowledge of how teeth work.

Publications

  • No publications reported this period