Team BLAZE
Bettering the Lives of Animals in Zoo Environments
Research Proposal
March 14, 2010
“I pledge on my honor that I have not given or received any unauthorized
assistance on this assignment.”
Logan Anbinder
Nikko Khuc
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Amy Cordell
Josh Lacey
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Gretchen Downey
Caitlin Moore
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Kelly Freudenberger
Emmarie Myers
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Shabaab Kamal
Samantha Roman
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Andrea Schmidt
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TABLE OF CONTENTS
Abstract……………………………………………………………………………………………3
Section 1: Introduction ……………………………………………………………………………3
Research Problem……………………………………………………………………...….3
Research Question………………………………………………………………………...4
Hypothesis………………………………………………………………………………...4
Project Justification…………………………………………………………………….…4
Section 2: Literature Review……………………………………………………………………...5
Enrichment ………………………………………………………………………………..6
Felids ...……………………………………………………………………………………7
Corticoid Analysis ……………………………..…………………………………….……8
Section 3: Methodology………………………………………………………………………….11
Experimental Design……………………………………………………………………..12
Data Analysis ……………………………………………………………………………14
Limitations ………………………………………………………………………………15
Section 4: Conclusion……………………………………………………………………………17
Works Cited………………………….……………………………………………………….….19
Appendices
A: Glossary………………………………………………………………………………22
B: Budget…………………………………………………………………………….......23
Table 1…………………………………………………………………………………...24
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Abstract
Wild animals, particularly felids, experience stress in captive environments that may lead
to disease and diminished fecundity. Enrichment has been shown to reduce this stress. In this
study, sensory, manipulative, and feeding enrichments will be added to the existing lion and tiger
exhibits at the National Zoological Park in Washington, D.C. Observational and hormonal data
will be collected and analyzed, and it is predicted that enrichment will result in decreases in fecal
corticoid levels and increases in non-stereotypic activity. By differentiating between the
effectiveness of multiple types of enrichment, we can determine the enrichment most suitable for
specific felid species and provide them with stimuli that encourage more natural behaviors.
Introduction
Research Problem
Despite the best attempts of the zoo community, animals’ enclosures will never be true
representations of their natural habitats because they are small and synthetic exhibits. As a result,
animals tend to use coping mechanisms known as stereotypies (or abnormal repetitive
behaviors) in order to relieve stress induced by the captive environment (Pitsko 2003). Stress
may cause reduced fecundity and can be detrimental to animals’ mental and physical health (Van
Metter et al. 2008). Captive felids are particularly susceptible to these adverse affects.
Additionally, when animals exhibit more natural behaviors they act as better representations of
their species in order to educate the public, serve as research subjects, and encourage greater
conservation. Solving stress-related problems is thus in accordance with three goals of the zoo
community, which are “conservation, research… [and] education” (Churchman 1987).
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Research Question
Our overarching research question is, “How do various types of enrichment, including
sensory, manipulative, and feeding, affect the activity budget and fecal corticoid levels of
felid species in a zoo environment?” We are testing the effectiveness of three different kinds of
enrichments on two species of felids to assess which techniques are most effective in improving
the quality of zoo animals’ lives. This improvement may be manifested in a more diversified
activity budget and a decrease in stereotypies, if they are present.
Hypothesis
When enrichment of any type is added to the husbandry schedules of captive lions
(Panthera leo) and tigers (Panthera tigris sumatrae), we hypothesize that there will be a
difference in both the activity budgets and fecal corticoid levels of the subjects compared to the
baseline (Skibiel et al. 2007). We expect that the animals’ fecal corticoid levels will decrease and
their activity budgets will show more diverse behaviors, as well as generally higher levels of
activity (Wielebnowski and Watters 2007). We also anticipate interspecific variance dependent
on the type of enrichment, due to physiological and temperamental differences between lions and
tigers (Van Metter et al. 2008).
Project Justification
Existing literature has determined that fecal corticoid levels are not always indicative of
high, negative stress levels (2009 email from Nadja Wielebnowski to authors; unreferenced) and
should not be used as the only measure of well-being. In addition to fecal analysis, direct
observation can also be used to quantify stress levels (Skibiel et al. 2007). Therefore, this
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research is novel in its combination of behavioral and hormonal indicators of stress levels,
providing observational and physiological support for our claims. Additionally, little research
has been done comparing the effectiveness of different classes of enrichment on individual
species (Van Metter et al. 2008). This research will allow for broader generalizations about the
effects of specific enrichments by using two felid species.
Our research focuses on felids because of the negative effects that stress has on these
captive animals’ fecundity (Terio et al. 2004). Previous studies suggest that decreased fecundity
is linked to a heightened endocrine stress response, and we hope that by learning how to lower
stress levels of captive felids, we will be able to understand how to more efficiently encourage
felid reproduction in captivity (Jurke et al. 1997). Increasing felid fecundity will consequently
aid zoos in their goal of conservation by providing subjects that most closely resemble their wild
counterparts, and will further zoos’ additional goals regarding research and education (Ogden
and Heimlich 2009).
Literature Review
As research has been conducted on the behavior of animals in captivity in the past,
decision making processes in the zoological community have accordingly become more
enlightened with regard to animal welfare. Zoos have successfully manipulated many factors,
such as social density, housing design, and degree of autonomy, in order to provide more
stimulating environments for animals in zoos (Maple 2007). Behavioral enrichment is one such
factor often utilized to create an atmosphere of “activity, novelty, and flexibility” (Maple 2007),
especially for felids. Behavioral enrichment may reduce stress levels in captive felids that often
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lead to a wide array of vascular diseases, diseases which are generally observed only in captivity
(Munson, 1993; Munson and Bolton, 1999).
Enrichment
Enrichment is the dynamic process that structures and changes an animal’s environment
in a way that provides for behavioral choices and elicits species’ natural behaviors and abilities
from the animal (Van Metter et al. 2008). Enrichment activities for felids can vary from exposing
animals to stimuli such as frozen zebra dung and piñatas, to providing exercise courses and chase
games (Van Metter et al. 2008). Studies have been conducted using different forms of
enrichment in many different species, all with the goal of determining the effects of
environmental changes on animal responses.
For example, studies have shown that different felid species may vary in their reactions to
enrichment activities, and slight environmental changes may alter specific biological functions,
like eating patterns and reproductive hormone secretion (Skibiel et al. 2007; Clubb and Mason
2007). Van Metter et al. (2008) found that using frozen blood balls, fresh zebra dung, scented
squash, and cardboard boxes had a substantially greater beneficial effect on African lions than on
the Sumatran tigers. The African lions exhibited more active behaviors and slept less than the
Sumatran tigers during the enrichment trials. The researchers also found that the animals did not
habituate to the enrichment over the trial period.
Moreira et al. (2007) found that changes in environmental enclosures caused the
reproductive cycle in female tigrinas (Leopardus tigrinus) and margays (Leopardus wiedii) to
change drastically. In this study, the two species differed in their physiological responses to
environmental change. After being placed into a large environment, the animals were transferred
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to a smaller enclosure. During the transfer, corticoid levels were measured to analyze the impact
on estrogen and fertility cycles because corticoid and estrogen levels have been shown to be
correlated. While fecal corticoid levels increased for both species, the effect was significantly
greater for margays than for tigrinas.
Felids
The literature is abundant with studies showing the effects of captivity on the welfare of
animals (e.g., Davey 2007; Clubb and Mason 2007; Terio et al. 2004). It has also been shown
that felids cope with captivity particularly poorly. In a multi-species study of infant mortality
rates of animals in captivity, three of the four most at-risk species were felids (Clubb and Mason
2007). In addition, most large felids are solitary carnivores, making the introduction of mates a
potentially dangerous process that often leads to fighting, injury, or death (Shoemaker et al.
1997).
The most common technique to enhance the welfare of captive animals is the use of
enrichment, but large felids have proven to be particularly resistant to the effects of enrichment
due to their naturally complex behaviors (Mellen and Shepherdson 1997). Additionally,
temperament and personality have been proven to play a factor in a felid’s response to
environmental enrichment (Boissey et al 2007). Different dispositions among individuals may
lead to different behaviors and coping mechanisms in reaction to the same stimulus
(Wielebnowski 1999). The level of fearfulness in animals has also been the subject of several
studies. For example, one study illustrated that Merino ewes with a calmer temperament produce
better quality milk and exhibit improved immune function and growth rate as compared to
Merino ewes with a more fearful disposition (Boissey et al 2007). One study that focused on
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cheetahs found that female cheetahs tended to have more fearful temperaments than males, and
non-breeding cheetahs tended to be more fearful than breeding cheetahs (Wielebnowski 1999).
The more fearful cheetahs tended to cope worse with the captive environment than those with
less fearful temperaments, suggesting that the fearful individuals might require more hiding
places in their exhibits (Wielebnowski 1999).
Additionally, the lack of space in zoo environments makes it difficult to accommodate
felids’ large ranging tendencies. Wide-ranging felids are accustomed to experiencing new
environments frequently; therefore, static zoo environments impede the exhibition of natural
behaviors. Furthermore, felids’ natural methods of hunting prey cannot be exercised due to the
ethical and public concerns with live prey (Pitsko 2003). Mellen and Shepherdson (1997) found
that cats quickly habituate to novel conditions, meaning that enrichment must be constantly
altered and reintroduced in order to be effective in encouraging more natural behaviors. Lions
have some of the most expansive ranges of the large felids, a factor that has contributed to a lack
of reproductive success in captivity with infant mortality rates nearing 50% (Shoemaker et al.
1997; Clubb and Mason 2007). We are focusing on such species because we hope to facilitate
more successful breeding in captivity and an increase in natural behaviors.
Corticoid Analysis
Fecal corticoid measurements are often used to monitor changes in animals’ stress levels.
Because of the physiological connection to stress and the benefit of being non-invasive, fecal
corticoid measurements have been implemented in many studies evaluating the effects of
enrichment on an animal’s level of stress (Wielebnowski 2009). Through a chain of
physiological events beginning with a perceived stressor, an animal’s body eventually secretes a
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stress hormone corticoid which can be measured in the animal’s feces (Graham and Brown
1996). Corticoids are part of the hormonal response of the physiological stress reaction, and are
excreted as waste in the feces. Therefore, measurements of hormonal levels in fecal samples can
provide useful information about the activity of the hypothalamic-pituitary-adrenal axis
(Wielebnowski 2003).
Because of the ability to monitor stress responses practically and non-invasively, fecal
corticoids are preferred over other methods such as blood sampling and urinary corticoid
measurements. Though blood samples show instantaneous changes of various hormones related
to stress, the simple act of collecting samples can actually increase stress in the animal and create
a confounding variable. Urinary corticoid measurements, like fecal corticoid analysis, are also
non-invasive, eliminating the possibility of inducing stress through sample collection. However,
the practicality of this approach is limited because cats tend to spray, making it difficult to
collect uncontaminated urine in sufficient quantities for analysis. A study of corticoid
metabolism in domestic cats also showed that fecal corticoids better reflected the actual
concentrations of stress hormones within the cat bloodstream than urinary corticoid
measurements (Graham and Brown 1996).
Fecal corticoids are measured with immunoassays, and all assays must be validated
before use to ensure that the hormones of interest are measured accurately. It is vital to the
integrity of any study that all assays and extraction techniques “detect biologically meaningful
alterations in the endocrine status of the animals” (Touma 2005). Validation is comprised of two
major aspects: analytical and physiological validity. Analytical validity refers to the sensitive of
the assay to different levels of hormones, as well as the general accuracy and precision of the
assay (Palme 2005). This can be established by using the assay to analyze several different
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dilutions of the relevant hormone, and ensuring that the assay reflects the correct level of the
hormone.
Physiological validity refers to the assay being responsive to actual changes in circulating
hormone levels. Establishing physiological validity involves pharmacologically inducing
changes in corticoid levels in the bloodstream and assessing if the assay reflects those changes
(Touma 2005). This is done by taking samples before and after events known to induce
glucocorticoid change (e.g., exogenous administration of ACTH, stressful events such as
veterinary exams) and seeing if the assay detects a marked change in hormone levels as a result.
Validation, like all assay testing, is subject to individual fluctuations, particularly between
genders and life-history stages, and as such, needs to be done with a large sample to eliminate
such variation (Palme 2005).
Though fecal corticoid levels can provide important data, the results cannot serve
as the sole basis for conclusions regarding an animal’s stress level. This is because corticoid has
a natural circadian rhythm that fluctuates throughout the course of the day and corticoid levels
vary widely among individual animals. Measurement of fecal corticoid levels is an average
measurement of this fluctuation. There are many factors within the nervous system, including
regulation of the neurotransmitters involved in the stress response, which may alter corticoid
levels in the feces. Additionally, normal corticoid ranges vary between individual organisms, as
every animal is biologically different. High corticoid levels indicate the presence of stress, but it
is impossible to differentiate between eustress, which might be the result of increased activity or
interaction with other animals, and distress, which may result from anxiety and boredom
(Wielebnowski 2009). Also, there are several limitations on sample reliability. These include the
freshness of the sample, possible environmental contamination of the sample, and urine
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contamination of the sample that may occur when another animal tries to mark its territory
(Wielebnowski and Watters 2007). Fecal corticoid measurements alone are thus insufficient for
making conclusions about the overall stress level of an animal. In order to compensate for such
limitations, corticoid measurements are most valuable when analyzed in the context of additional
data, such as behavioral data.
Methodology
We will conduct our research at the Smithsonian National Zoological Park in
Washington, D.C. using Sumatran tigers and African lions during the summers of 2010 and
2011. We will conduct pilot testing in the beginning of the first summer to determine the
schedule that best fits with established zoo protocols and husbandry practices. We will use a
within – subject design, which involves collecting data before, during, and after implementation
of the enrichment, allowing each felid subject to serve as its own control by providing its own
baseline (Graziano and Raulin 2007).
Timeline for Individual Trials
Experimental Design
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There will be two trials for each of the three types of enrichment, with each trial lasting
five consecutive days. These six trials will take place during the first summer of research in
2010. We will observe each animal’s behavioral responses to the enrichment and collect fecal
samples for later analysis. Behavioral observation will be conducted at the same time each day
in order to account for the potentially confounding effects of circadian rhythm on activity levels
(Liu et al. 2006). Observations will be quantified based on the duration and frequency of each
behavior exhibited, and an activity budget for each animal will be constructed for each time
period (baseline, during enrichment, and after enrichment). These activity budgets will then be
compared to determine if our enrichment results in altered activity levels or activity budgets.
We will also complete research during the summer of 2011 during which each trial will
involve a combination of enrichments. This will involve a combination of sensory, manipulative,
and feeding enrichment. For example, we could supply a manipulative object such as a
cardboard box and have inside of this box a unique food object. The methodology will remain
the same, but there will be an added level of complexity to the enrichments that are introduced.
We will compare the data collected during the more complex trials with values collected from
the first summer.
Pilot Testing
Before beginning experimental manipulation, we will conduct pilot testing to establish
the normal patterns of behaviors and hormone secretion for each animal. We must determine the
degree to which hormone levels fluctuate naturally before attempting to determine if our
experimental manipulation incited the changes. For three weeks before applying our
enrichments, we will observe all potential subjects at different two-hour intervals throughout the
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day. Time of observation will be randomized for this trial period in order to eliminate seasonal
confounds. This will allow us to establish the optimal time, determined by the presence of
stereotypic behaviors, to conduct our experiment with enrichment. At the conclusion of the
observational period, we will analyze all of the daily fecal samples in order to characterize
normal corticoid levels and daily fluctuations. During this time, we also plan to conduct at least
one inter-observer reliability test in order to make sure all observers are quantifying observations
accurately and consistently.
Establishing Baseline
Once we begin our experimental manipulation, we will establish the baseline activity
budget and fecal corticoid levels for each animal for the week. Baseline observational data will
be collected for each animal on Day 1 and Day 2, during the optimal time determined in pilot
testing. In order to establish the baseline fecal corticoid levels, the zoo staff will collect all
available fecal samples from Day 1 and Day 2. To allow for individual identification of fecal
samples, plastic pellets in a color unique to each individual will be added to each animal's food
in the days prior to fecal sample collection.
Enrichment Application
On Day 3, one type of enrichment will be added into the exhibit when our subjects are
present. The order in which each type of enrichment is provided to the animal will be
randomized to prevent habituation to a particular pattern of testing. After implementing the
enrichment, we will observe the animals’ behaviors, using the same techniques described for
baseline data collection. The enrichment will stay in the enclosure for the remainder of the day.
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We will collect all available fecal samples each of the five days, and our behavioral observations
will continue on Day 4 and Day 5. This period should allow us to document the return of
behavior and corticoid levels to baseline before the next trial begins. This procedure will be
repeated for the remainder of the trials.
During observations, we will record the type and duration of each behavior expressed by
the study subjects using JWatcher software, which allows for compilation and analysis of
behavioral data. The observers will record specific behaviors, which will later be classified by
category. These categories will be defined by an ethogram. Our activity budgets will be
established from the results of pilot testing.
Data Analysis
For each animal, we will compare the duration of active, inactive, and stereotypic
behaviors as well as the overall activity budget before, during, and after the implementation of
the enrichment. Data collected with JWatcher will be used to test for statistical differences
between the three periods of observation. The baseline activity budget will be compared to the
activity budget from Day 3 in order to identify which type of enrichment most increases active
behaviors while decreasing stereotypic and passive behaviors. Data for each species will be
analyzed separately to determine the most effective type of enrichment for each species.
Because of the similar body types of the two field species, we may be able to generalize to
similar-sized felids should strong similarities exist between the data sets.
The fecal corticoid analyses will be conducted at the Department of Reproductive
Sciences at the Smithsonian National Zoological Park, using established protocols. Fecal
samples will be analyzed by extracting the corticosterone from the sample, then using previously
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validated enzyme immunoassays to determine corticosterone concentrations. We will analyze
fecal corticosterone levels and activity budgets for each animal, and examine the corticosterone
levels for overall trends throughout the trial period.
Limitations
A significant limitation of this study is that much of the data collection depends on the
animal husbandry schedules; therefore the specific time periods of data collection and
enrichment introduction are subject to change based on input from zoo staff. Additionally,
changes to the enclosure or to the daily schedule of the felids that are outside of the team’s
environmental manipulation techniques could have a significant impact on the results. If the zoo
staff were to change the feeding schedule of the felids, or add or remove objects from the
enclosures, the team would be unable to attribute changes in the activity budget or fecal corticoid
levels to the enrichment techniques we implement rather than the changes made by the zoo. If
this were to happen, we may draw incorrect conclusions about the effectiveness of the
enrichment items that we manipulated.
The various ages and genders of the felids also present a limitation, because they result in
the formation of social groups, requiring them to be on exhibit at different times of the day.
Therefore, we must consider the rotation schedule at the zoo in our plans, so that we have a
consistent group of felids to test and monitor. If data is collected from felids immediately after
they are transported to the zoo from other facilities, the fecal corticoid data levels will be
skewed, as corticoid levels can increase dramatically for almost two weeks after time of
relocation of the animal (Dembiec et al. 2004).
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Another potential limiting factor is individual personality differences in the lions and
tigers. An animal’s temperament affects its ability to cope with captive environments and novel
situations (Wielebnowski 1999). For example, the subjects’ personalities may be more
aggressive, calm, fearful, or excited. This will affect how each animal responds to the enrichment
items, and animals with different personalities will react based on their own personality traits.
We may not know if a subject is not interacting with the enrichment item because of its
temperament or because the enrichment item fails to elicit active behaviors. Talking to the zoo
staff who work with the lions and tigers on a regular basis will help decrease individual
temperament as a confounding variable. We will have to know each animal’s personality based
on its interactions and observations by the zoo staff before conducting our studies. The
personalities will also be taken into account when analyzing the effectiveness of the enrichment
trials.
Because one of the main methods of data collection is through observation of the felids’
behavior, differences between observers’ perceptions of the behavior could cause discrepancies;
however, the design of our experiment reduces inter-observer bias. We will attempt to minimize
such bias and inconsistencies by testing inter-observer reliability during pilot testing. Finally,
defining specific behaviors with an ethogram will decrease observer bias, and the data will be
more reliable.
Due to seasonal variability, weather presents an additional variable. Since fecal corticoid
levels vary throughout different seasons in felids, we will establish a baseline for each felid per
trial to eliminate seasonal fluctuations as an extraneous variable (Wielebnowski and Watters
2007). Because weather cannot be accurately predicted in advance, inclement weather may
interfere with data collection and animal behavior. A note of basic weather conditions (e.g.,
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temperature, precipitation) will be made when collecting data, so that this can be accounted for
in subsequent statistical analyses.
The characteristics of visitor activity including density and level of activity of the visitors
have been proven to alter animal behavior both in positive and negative ways (Davey 2007).
Because visitor levels at the zoo cannot be controlled, a new extraneous variable is introduced
into the experiment. Visitor levels might cause fluctuations in animal behaviors or fecal corticoid
levels that interfere with our data, causing uncertainty in determining whether the introduced
enrichment caused the fluctuation. By conducting our research on weekdays only, we aim to
decrease the effect of differing visitor levels. However, we will collect data from the zoo
regarding the number of visitors each day of our research, in order to take this factor into
consideration.
Illnesses and genetic ailments cannot always be prevented, and may present as an
additional confounding variable in our study. If a felid were to become ill during the study,
corticoid levels could fluctuate based on the illness rather than our manipulations. The behavioral
observations and records should also reflect the effects of the illness on the felid’s activity
budget. Data from any ill animal will be excluded from our final analysis.
Conclusion
In general, felids are more susceptible than other common zoo species to the adverse
effects of stress in a captive environment. This is a particular cause for concern due to the
necessity of conservation and preserving genetic diversity within these species. Additionally,
animals that act naturally are better tools for education, and more likely to attract visitors than
those that act stereotypically or lethargically. We plan to combine behavioral observation and
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corticoid level analysis in order to provide valid indications of stress levels in the animals
studied. Through the novel combination of behavioral and physiological data, we will study the
effects of sensory, manipulative, and feeding enrichments on two different felid species, in order
to determine which method is most effective in stimulating active behaviors while
simultaneously reducing stress levels for each species. We believe that our results can be
generalized to other zoos, providing valuable information to animal care experts about ways to
improve the well-being of captive felids.
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Appendix A: GLOSSARY
Activity Budget: A tool used to illustrate the frequency of previously defined behaviors that are
exhibited by the subjects (MacDonald 2009).
Enrichment: A way of “[increasing] the complexity of the captive environment and possibly
[enhancing] captive animals’ well-being by stimulating active behaviors and reducing
stereotypical behaviors commonly seen in zoo felids” (Skibiel 2007).
Enzyme Immunoassays: An assay technique that utilizes enzymes as reporter labels to measure
analytes within a sample (Lequin 2005).
Feeding enrichment: “a variety of task oriented puzzle feeders and different methods of
presentation encourage animals to think and work for their food, as they would in the wild”
(Hogle 2009)
Manipulative enrichment: “items (such as barrels, balls, or boxes) that can be manipulated in
some way via hands, mouth, legs, horns or head simply for investigation and exploratory play”
(Hogle 2009)
Ranging Tendency: the average distance a species travels in a given period of time in a typical,
natural setting (Terio et al 2004)
Sensory enrichment: “techniques such as bubbles, scents, or video recordings that would
stimulate…the animals’ senses- visual, olfactory, auditory, taste and tactile” (Hogle 2009)
Stereotypies: Abnormal repetitive behaviors exhibited by animals, often in response to stress;
also known as stereotypic behaviors (Pitsko 2003)
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Appendix B: BUDGET
Expenses
Cost
0.00
~400.00
~400.00
0.00
JWatcher Software (available online)
Manipulative enrichment materials
Feeding enrichment materials
Sensory enrichment materials
(Animal scents will be provided by the Zoo)
Fecal Corticoid Immunoassay Kits
(45 samples/animal x 12 animals at $7/sample)
Round trip transportation to the zoo from College Park
(5 observers x 55 days/observer x $5/trip)
7560.00
2750.00
Total
11110.00
*For two summers of research
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Table 1. FELID BEHAVIORS*
Active Behaviors
Feeding
Social interaction
Locomotion
Alone play
Rolling
Swimming
Alert
Scent marking
Vocalization
Eating, drinking, chewing, or licking edible substances
Engaging in behavior towards another, including social grooming
Walking, running, climbing
Partaking in playful activities alone
Rotating side to side while laying down
Any activity done in the water
Eyes open and aware of surrounding, not engaged in other
activities
Releasing spray from posterior on an object or area
Making noises with the mouth
Inactive Behaviors
Sleeping
Laying down
Sitting
Grooming
Urinating/defecating
Laying down with eyes closed
Laying down with eyes open, not alert
Hind legs on ground, upper body upright, not alert
Licking or scratching itself
Projection of bodily fluids other than scent-marking
Stereotypic Behaviors
Pacing
Biting at fur
Walking a regular bath repetitively, path may be well worn
Biting at fur, outside of self-grooming behaviors
* ethogram modeled from Skibiel et al. (2007) and Van Metter et al. (2008).
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