Major Grant Proposal 2010

Variation in pocket gopher (Thomomys) digging morphology as a

determining factor in species distribution in northeastern California
Ariel Marcy

Proposal Summary

Western pocket gophers (genus Thomomys) are subterranean rodents that use tooth- and

claw-digging to tunnel underground. Each species’ range is determined through

interspecific competitive exclusion such that two species of gopher rarely occupy the

same area. My objective is to test whether variations in the Thomomys digging apparatus

can explain why each species gains competitive dominance in the particular soil and

climate conditions of its range. I will approach this question by comparing gopher

functional morphology, and species location with respect to soil and climate

characteristics. Understanding the interaction between gopher morphology, soil, and

climate could help to explain the current distribution pattern of Northeastern Californian

species of pocket gophers, provide a mechanism for a species turnover event during the

Pleistocene, and predict gopher distributions under a climate change model.

Objective

Pocket gophers (family Geomyidae) are subterranean rodents that use tooth- and claw-

digging to varying degrees to tunnel underground. Western pocket gophers (genus

Thomomys) are distributed throughout the western U.S. Thomomys inhabit a wide variety

of habitats and exhibit huge interspecific morphological variation. Pocket gopher ranges

are determined through competitive exclusion such that two species rarely occupy the

same area.
 My objective is to combine species locality and morphology analyses to test

whether variations in the Thomomys digging apparatus can explain why each species

gains competitive dominance in the particular soil and climate conditions of its range. I

hypothesize that morphological variation between the digging apparatus of the species

determines their niche along the tooth-to-claw-digging strategy spectrum. I will test this

using morphometrics, quantitative shape analyses, on gopher skeletal specimens.

I predict that these differences contribute to the competitive dominance of one

species over another under certain soil characteristics (e.g. particle size, hardness, water

capacity), many of which vary with climate. I will test this by projecting the latitude and

longitude of gopher capture site data onto maps of soil and climate characteristics.

My final aim is to combine the results to propose a biomechanical explanation of

how gopher morphology determines each species’ competitive ability under certain soil

and climate characteristics. This knowledge could help explain the current distribution

pattern of Northeastern Californian species of gophers, understand a species turnover

event during the Pleistocene, and predict gopher distributions under a climate change

model.

Background and Significance

Charles Thaeler laid the groundwork for pocket gopher research in Northeastern

California by investigating the claim that gopher ranges never overlap. Thaeler chose

Northeastern California because five species inhabit this area and of the ten possible pair-

wise species overlap combinations, nine occur. He created a distribution map for NE

California through extensive field observations and sampling (Fig 1). He determined that

Thomomys have abutting ranges, but species almost never exist sympatrically (19). The
rare cases of range overlap occur in areas with two radically different soil types.

Morphological differences had not been analyzed thoroughly by Thaeler’s time but he

suggested these as the main reason for competitive exclusion (19).

Fig 1: Distribution map of Thomomys genus pocket gophers, for reference, top border is
Oregon, right border is Nevada (from Thaeler 1968)

Thaeler’s hypothesis for exclusion assumes that variations in environmental

characteristics across the NE Californian region alter the outcome of competition. To test

this, my study will combine species locality and morphology analyses to see whether a

biomechanical advantage under particular soil and climate conditions can explain the

geography of range boundaries between competing gopher species. Extensive

documentation of gopher sensitivity to soil moisture, temperature, and texture supports

this hypothesis (13,16). Digging is very energetically demanding, but the exact cost

varies between soil types (11). Furthermore, metabolic rates of subterranean species

working in harder soils vary, demonstrating that some are more efficient in particular soil

types (12).
 Recent assessment of gopher morphology has emphasized the dual nature of the

digging apparatus, involving both the forelimbs and the jaw, which are the lever arms for

claw- and tooth-digging respectively (10). Further analysis of the digging apparatus

found that claw-digging tends to restrict animals to friable sandy soils whereas tooth

specializations broaden the potential spectrum of habitable soil textures (10). The authors

conclude that digging specializations contribute to the realized range of gophers,

however, the exact mechanisms are undeveloped.

In a follow-up study, Lessa and Stein conducted linear morphometric and

myological analyses that included two representatives from the genus Thomomys. The

morphometric analysis found only osteological variation between jaw and forelimbs (9).

This observation allows me to limit my morphological studies to skull and forelimb

bones, which are much more accessible than myological material. Their analyses also

showed that Thomomys morphology varies from highly specialized for tooth-digging to

slightly favoring claw-digging (Fig 2).

 Fig 2: PCA illustrating how genera and two species of Thomomys spread on axes of size

and claw- or tooth-digging traits (From Lessa and Stein 1992)

Despite the large number of morphological studies on pocket gophers, no studies

have focused only on differences within genera and thus range determination between

species is still poorly understood (14). The existing literature draws on the larger cross-

genera morphological differences to characterize gophers as more specialized for claw-

digging versus tooth-digging – invaluable information for my project. However,

unwarranted generalizations from one species to its entire genera are common in pocket

gopher literature. Despite the spread in Thomomys digging modes noted in Lessa and

Stein 1992, the genus is usually characterized as tooth-specialized diggers in cross-genera

studies, and strangely, Stein describes them as claw-diggers in Stein 2000.

Morphological comparisons within any pocket gopher genera would generate

interesting results to a field lacking such studies. Thomomys is an ideal genus to

investigate sub-genera differences because its species vary within an order of magnitude

in size and they inhabit a wide range of soils and habitats (18,19). Most of the cross-

genera studies described above used linear morphometrics. My approach will achieve a

higher degree of sensitivity by adding geometric morphometric analysis.

My focus on interspecific differences allows me to introduce a unique extension

to gopher ecology. Previous cross-genera studies made observations of the general

ecology for the genera, but extensions are limited because each genera of gophers reside

in different regions of the country. Therefore the populations studied do not interact and

comparisons cannot control for larger variations between ecosystems nor for variations
within the genera. I avoid these issues by focusing on all the species within one genus

located specifically in Northeastern California.

If both facets of my study reveal significant results, these will be combined to

propose a biomechanical explanation for the competitive exclusion determining pocket

gopher spatial distributions. Knowledge of why particular gopher species competitively

exclude the others in certain soil types and that of ancient gopher distribution information

could be extended to recreate ancient regional climates. There is evidence of a gopher

replacement event in Northeastern California during the Pleistocene in which one species

supplanted another from its former range (3). We will be able to describe how climatic

conditions might have changed during the Pleistocene, once we understand the soil and

climate conditions these species thrive in.

Furthermore, this knowledge, in conjunction with climate change models, could

be used to predict future gopher distributions under different parameters. Gophers are

ecosystem engineers that create habitats for endangered species, such as the burrowing

owl, reduce invasive grass establishment, and otherwise greatly affect community

structure (4,6,7,18). Forming a deeper understanding of pocket gopher species

biomechanics, competitive interactions, and ecology will generate insights into the past,

current, and future Californian ecosystem.

Methodology

I will use two types of morphometric analysis, linear and geometric, to quantify

functional differences between the skulls and forelimbs of the five species of Thomomys

pocket gophers from NE California. I plan to work with the Hadly lab technician to use

GIS to overlay museum specimen locality data on soil, rock strata, temperature, and
rainfall maps. I will use Principal Components Analyses (PCA) to determine whether

correlations exist between the soil and climate, and the observed spatial distribution

pattern.

Morphometrics is a quantitative way of comparing shape. Linear morphometrics

(LM) are simple measures of length and width of bones and bony processes (muscle

attachment sites). I will use five forelimb and eight cranial and dental standard

measurements previously described for gophers (Fig 3). My specific predictions for

variations in linear measurements by digging mode are described in Table 1. LM can be

used on ancient bones and will generate absolute measurements appropriate for

quantitative biomechanical studies of gopher lever arms. Often morphometric studies on

species within a genus produce data that can be used to identify ancient bones more

specifically.

Fig 3. Measurements for morphometric analysis (from Lessa and Stein 1992)
Table 1: Linear morphometrics measurements, abbreviations, grouped by expected
changes for each digging mode
Measurement Abbr. Claw-digging
Humerus length HUML Decreased (higher forces experienced in arms)*
Deltoid process DELTW Increased (greater muscle attachment)2
Width of epicondyles EPICW Increased (greater muscle attachment)2
Length of ulna ULENG Increased (due to increase in OLCER)*
Olecranon process OLCER Increased (greater lever for triceps)*
Basilar length of skull BAL Decreased (dorsal flattening leads to greater
surface area for muscle attachment)*
Zygomatic breadth ZB Increased (more surface area for jaw muscles)*

Measurement Abbr. Tooth-digging

Rostral width RW Decreased (smaller cross-area of incisors decrease
R)1
Rostral breadth RD Increased (elongated to increase procumbency)2
Width of incisors INCW Decreased (smaller cross-area of incisors)1
Length of diastema DIAST Increased (indicator of procumbency)2
Vertical width of incisors INCL Increased (indicator of procumbency)2
Distance from tip of incisor to BASE Increased (indicator of procumbency)2
base of first molar
Rationales for predictions were adapted from Lessa 1990 (denoted by 1), Lessa and Stein 1991
(denoted by 2), or extensions were made from Stein 2000, which was not specifically discussing
differences between modes of digging but subterranean adaptations in general (denoted by *)

I will continue to acquire gopher skeletal specimens from the Museum of

Vertebrate Zoology (MVZ) at University of California, Berkeley. Only individuals

collected from Northeastern counties will be used in order to control for regional

variation across the state. I aim to measure at least 25 specimens per species, which has

worked in previous morphometric studies in rodents (1,5,21,22).

Using digital calipers, I have completed forelimb measurements for nearly 100

individuals including all five species. Redundant measuring allowed me to assess whether

my measurement error was below 5%. I was not able to measure one specific

measurement consistently with calipers so I plan to take digital pictures of my specimens

and use ImageJ to retake them. Using R, a statistical program, I have completed a

preliminary PCA analysis of the five species by the four accurate measurements of their

forelimbs (Fig 4,5). PCA is a mathematical procedure that transforms a number of

possibly correlated variables into a smaller number of ranked uncorrelated variables

called principal components (21). In morphometrics, the first PC usually describes size

and the succeeding PCs account for shape. The results show separation of species by size

and they suggest that more powerful analyses will find significant shape differences. I

will complete a more extensive statistical analysis of these data as part of my final project

for Biostatistics this quarter.

Fig. 4. PCA of my preliminary linear measurements. PC1 is correlated with size.

 Fig 5. Scatter plot of P21 versus deltoid width shows that PC2 is moderately correlated to
variation in the deltoid process.

Geometric Morphometrics (GM) is a branch of mathematical shape analysis aided

by digital camera and computer software. GM can perform more sophisticated analyses

than LM because linear measurements do not convey information about spatial

relationships between measurement points (21). GM solves this problem by creating a

digital network of points called landmarks that define the shape of the bone of interest.

Landmarks must be discrete points on an organism that are recognizable across all

specimens and can be pinpointed with a computer image of the specimen (Fig 6). Often,

recognizable areas have functional significance, such as a muscle attachment scar. I can

use the photos I take for LM analysies and ImageJ to perform most GM analyses. Our lab

computer has additional statistical analysis programs for regression, CVA, MANOVA,

and PCA tests.

 Fig 6: Landmarks for rodent mandible (From Zelditch and Swiderski 2009)

Because GM organizes landmarks into a matrix of interrelated points, each

specimen can be scaled to the same size, thus removing the variable that drove most of

the differences in the linear PCA and likely overshadowed variation due to shape. A PCA

of GM data creates vectors that indicate the direction of shape change across groups of

species (Fig 7). Landmarks could then be grouped using osteological or myological

adaptation indicators of digging mode previously described by cross-genera studies of

pocket gopher morphology. Analysis of how these elements vary could then be applied to

describe how Thomomys species fall with respect to each other on the claw- and tooth-

digging spectrum.

Fig 7: PCA results of landmark-based GM of a rodent cranium (From Zelditch and Swiderski
2009)

I will use the Geographic Information System (GIS) to test whether range

boundaries of species are correlated with particular soil and climate conditions by

projecting the latitude and longitude of each gopher capture site onto maps of soil and

climate. I can access precise maps of soil and climate characteristics for the NE
California region from the Natural Resources Conservation Service (NRCS) and United

States Geological Service (USGS). Gopher locality data for all five species of Thomomys

from museums in the Northwest region of the US can be accessed from both the Mammal

Networked Information System (MaNIS) and Arctos, a multi-institution museum

database. I plan to compare species locality data to soil, rock strata, temperature, and

annual precipitation maps.

Because regional environmental data does not come from a normal distribution,

results will be analyzed using non-parametric tests, which can be calculated in R. PCAs

can be used to analyze which environmental characteristics are most important for

generating the observed gopher species distribution pattern.

Resources and Preparation

My greatest resource is the Hadly lab. I entered as a rising sophomore in a field and lab

assistant position for a grad student studying the effects of ancient climatic change on

small mammal populations. Since fall 2008, I have met with Prof. Hadly at least once per

quarter to discuss a course of investigation that has evolved into this proposed study. The

early preparation gave me time to conduct a number of preliminary measurements and

analyses, which have informed my methodology and supported my course of action. With

assistance from Lily Li, the Hadly lab technician, I have started to use GIS to generate

qualitative data on the correlation of gopher locality and soil type

As a member of the lab, I participate in weekly lab meetings, and present on my

project once a quarter to receive feedback from Prof. Hadly and the lab’s post-docs, grad

students and undergraduates. This community draws from a wide variety of expertise

including GIS, geometric morphometrics, programming in R, biomechanics, and

extensive research with mammal skeletal material. The lab group is an invaluable

resource and my interactions with them have helped hone my research questions and

methodology.

The lab permit allows me to take out specimens from the MVZ, gives me access

to the camera set-up required for morphometric studies, and to the computers with the

necessary data analysis and GIS programs.

In January, I met with Prof. Scott Fendorf, a soil biogeochemist who offered to be

resource for me. Prof. Fendorf advised me on what aspects of soil to consider and

directed me to the NRCS soil survey datasets for my GIS analyses. In addition, he has

offered to coordinate a meeting with me, Prof. Hadly, himself, and visiting physical soils

scholar, Prof. Oliver Chadwick once I have more GIS results. I plan to take Prof.

Fendorf’s class on the Science of Soils next quarter.

Last quarter I took Performance, Development, and Adaptation of Skeletal

Muscle, which explored how the muscular and skeletal systems interact to generate

forces and how biomechanical studies are conducted. The class gave me a chance to

receive feedback on my proposal from Prof. Delp and two of his grad students who

specialize in biomechanics.

Next quarter, I plan to take the Natural History of the Vertebrates, which will

cover topics including physiology, behavioral ecology, community ecology and feature

labs on comparative skeletal morphology, including geometric morphometrics.

Other pertinent courses include Ecology, which covered species interactions,

competition, and climatic effects on populations, and Biostatistics, which has given me

greater facility with using statistical tests in R.

 This project will culminate in an honors thesis required for my concentration in

Ecology and Evolution within the Biology major. I plan to produce a paper for

publication as well as a poster to present at SURPS. I have also submitted a poster

abstract with preliminary findings to the 9th International Congress of Vertebrate

Morphology, which will be held in Uruguay, July 26th through 31st, 2010.

Timeline

Date Activity
Spring Determine GM landmarks, practice photographing specimens, familiarize
quarter GM methods, complete GIS analysis of gopher locality and soil survey data,
meet with Prof. Chadwick
Summer
Jun 29 Take photos of specimen jaws, ID landmarks
July 5 Take photos of specimen humeri and ulnae, ID landmarks
July 12 Statistical analysis of GM data
July 19 GIS analysis with precipitation, create poster for ICVM conference
July 26 Attend ICVM conference in Uruguay, present poster
Aug 2 Retake linear morphometrics with ImageJ
Aug 9 Analyze linear morphometric results, GIS analysis with temperature
Aug 16 GIS analysis with rock strata
Aug 23 Synthesis of GIS analyses
Fall Finish remaining analysis, start writing paper, create poster for SURPS
quarter

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