NM-Rs au Naturale: Investigations into Simulating a Natural

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NM-Rs au Naturale: Investigations into Simulating a Natural NM-Rs au Naturale: Investigations into Simulating a Natural

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NAKED MOLE-RATS AU NATURALE: INVESTIGATIONS INTO SIMULATING A

NATURAL ENVIRONMENT

1

NM-Rs au Naturale: Investigations into Simulating a Natural Environment

By

Jouvay (Jenna) Pantophlet

Submitted in partial fulfillment of the requirements for the degree of

Master of Arts in Animal Behavior and Conservation, Hunter College The City University of New York

April 28th, 2022

April 28, 2022 Diana Reiss

Date Thesis Sponsor

April 28, 2022 Daniel McCloskey

Date Second Reader


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Abstract

Naked Mole-rats (NM-Rs) have been studied in laboratories for decades due to their

unique behavior and physiology. However, due to the scope and complexity of the NM-R’s

natural subterranean tunneling system, it has been difficult to replicate in the laboratory

environment. From a researcher’s perspective, optimal housing is cost- and space-efficient and

easily cleaned. On the other hand, optimal animal welfare and husbandry encourages the most

biologically relevant enclosure to evoke the fullest range of an animal's behavioral repertoire.

While there is an abundance of works centered on the biomedical potential of these odd rodents

(Buffenstein et al, 2012; Delaney et al, 2016), there is comparatively little in the way of housing

and husbandry refinements; meaning that even basic welfare studies, like those done for the rat

in 1906 by the Wistar Institute, are likely non-existent for the NM-R. Even when remarked upon,

housing standards for NM-Rs seem to stand in stark contrast to their natural habitats. NM-Rs are

most often found in hard solidified lateritic loam soil but have also been known to inhabit pure

gypsum (Jarvis and Sherman, 2002). However, they are often kept in wood shavings, corn cob,

corn husks, grasses, or paper towel in captivity (Wood and Mendez, 2002; Suckow, 2012; Chenlin

et al, 2017). Here we hope to offer evidence in support of a new potential substrate for the NMR

in the laboratory setting that supports an increased biological relevance but can be implemented

quickly and cheaply.


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Table of Contents

Abstract ................................................................................................................................ 2

Table of Figures ..................................................................................................................... 4

Introduction .......................................................................................................................... 5

The Laboratory Environment and Biological Relevance ............................................................. 6

Differences Between Wild and Captive Populations of Animals ................................................. 9

Species of Interest for Improved Biological Relevance: The NM-R ........................................... 10

Design Features for the Improved Husbandry System .............................................................. 12

A Housing Substrate Candidate: Papercrete ............................................................................. 15 Portland Cement ................................................................................................................... 16 Newspaper ............................................................................................................................ 17

Specific Aims.............................................................................................................................. 18

Methods ............................................................................................................................. 19

Subjects and Facilities ............................................................................................................... 19 Housing ................................................................................................................................. 20 Cleaning Routine ................................................................................................................... 23

Materials ................................................................................................................................... 23

Data Collection .......................................................................................................................... 25 Behavioral Observations Method ......................................................................................... 27 Data Analysis ......................................................................................................................... 28

Results ................................................................................................................................ 29

Papercrete Durability Test ........................................................................................................ 29

Behavioral Data ........................................................................................................................ 32

Discussion ........................................................................................................................... 39

Papercrete Construction ........................................................................................................... 41

Microclimate Efficacy ................................................................................................................ 42

Behavioral Assessment ............................................................................................................. 44

References .......................................................................................................................... 48


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Table of Figures

Figure 1 – Examples of Modular Caging System …………………………………………………………………… 20

Figure 2 – NM-R Standing on Cob Substrate ………………………………………………………………………… 21

Figure 3 – Layout of Chambers for Colony Terrific ……………………………………………………………….. 22

Figure 4 – Layout of Chambers for Colony ……………………………………………………………………………. 23

Figure 5 – Soaking and Mixing of Shredded Newspaper in a Process Known as "Pulping” ……. 25

Figure 6 – Papercrete Molding and Casting ………………………………………………………………………….. 25

Figure 7 – Testing Chamber Locations ………………………………………………………………………………….. 27

Figure 8 – Block Weight Over Time – Linus …………………………………………………………………………… 29

Figure 9 – Test Block Day 1 vs. Day 15 – Linus ………………………………………………………………………. 30

Figure 10 – Block Weight Over Time – Terrific ………………………………………………………………………. 31

Figure 11 – Test Block Day 1 vs. Day 15 – Terrific ………………………………………………………………….. 31

Figure 12 – Duration Inside Test Chamber Regardless of Treatment by Colony …………………….. 33

Figure 13 – Average Duration Inside Test Chamber With Block by Colony …………………………….. 33

Figure 14 – Average Duration Inside Test Chamber With Block by Colony …………………………….. 34

Figure 15 – Percent of Observed Location by Treatment – Linus …………………………………………… 35

Figure 16 – Average Duration Inside Test Chamber by Treatment – Linus …………………………….. 36

Figure 17 – Average Duration Inside Test Chamber With Block by Crowding Density – Linus … 36

Figure 18 – Average Duration Inside Test Chamber w/o Block by Crowding Density – Linus ….. 37

Figure 19 – Duration Inside Chamber With Block by Crowding Density – Linus ……………………… 37

Figure 20 – Percent of Observed Location by Treatment – Terrific ………………………………………… 38

Figure 21 – Average Duration Inside Test Chamber by Treatment - Terrific ………………………….. 39


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Introduction

Housed at the Animal Facility at the College of Staten Island (CSI) since 2010 are eight

Naked Mole-rat (NM-R) colonies that participate in various behavioral and biomedical research

projects in Dr. Daniel McCloskey’s laboratory. These colonies are currently housed in a tailor-

made modular artificial burrow system comprised of square and rectangular polycarbonate

steam pans with fitted lids, connected by polycarbonate tubes and littered with loose corn cob

bedding. From a researcher’s perspective, this is an ideal housing system. It is cost- and space-

efficient, relatively easy to clean, and provides quick visualization of, and access to, individual

animals. However, optimal animal welfare and husbandry encourages the most biologically

relevant enclosure possible to encourage the full range of an animal's behavioral repertoire. NM-

Rs maintain intricate and complex natural habitats, which have been difficult to replicate in the

laboratory environment, so this current system represents a compromise between researcher

needs and the ecological needs of the animals.

From the perspective of a laboratory animal technician working at CSI, this system

requires a labor-intensive, 48-hour cleaning process that poses several occupational health risks.

The ‘tunnels’ between the steam pan ‘chambers’ are tailor-made, hand-threaded PVC tubing.

Although functional, the threads on these tubes and all their connecting pieces are prone to

imperfections, warping, and friction sealing to an impressive degree if not threaded properly.

These factors mean that breaking down and setting up any one colony results in hundreds of

strenuous wrist rotations, putting the technician at great risk for repetition injury. In fact, one of

the main care staff for these animals has undergone carpal-tunnel surgery in both wrists due to


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the difficulty of working with the tubing, and the rest of the team rely on a strict regimen of wrist

stretches and braces to manage symptoms.

For some time, Dr. McCloskey and the animal care staff have looked for a way to improve

the husbandry situation of the NM-R colonies in hopes of finding materials and methods which

take less time to complete, are ergonomically safer for the technicians, and are more ecologically

and biologically representative of the native habitats of these animals. Here, we hope to

investigate the efficacy of a new potential substrate for the NM-R in the laboratory setting that

can increase the standard of welfare but can be implemented quickly, cheaply, and safely.

The Laboratory Environment and Biological Relevance

As Newberry (1995) suggests, it is necessary to assess the extent to which animals in

captivity possess behavior that “resemble that performed in a more extensive or natural

environment”. A captive environment is a living-space with well-defined boundaries, where an

animal is dependent on human intervention for many or all its basic needs. This contrasts with

the wild state where, even though they may be restricted by geographical barriers, animals can

freely move through the world and acquire basic needs entirely through their own efforts (Poole,

1991).

The concept of welfare itself is complex, and since animals cannot report on their own

quality of life the way humans can, we are limited in our interpretation of their welfare as a

mirror of our own. As described by David Fraser (2008), this reality has produced three large and

overlapping lenses through which researchers attempt to study animal welfare: 1) health and


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functionality, 2) the ability to behave naturally, and 3) the affective state of an animal. Fraser

concludes by suggesting that an ideal measure of welfare takes all three of these factors into

account and finds the answer somewhere in the middle. However, these three aspects

frequently contradict one another, making real world application a constant balancing act. The

current laws and guidelines regarding research-animal welfare outline minimum standards that

aim to avoid animal suffering but, if followed exactly, merely allow the animal to cope with its

captivity rather than thrive in it (Maple and Bocian, 2013). Established dogma in animal

caretaking communities can frequently play a role in these standards despite a lack of empirical

evidence (Loughman, 2020).

Animals that have evolved in a particular environment will have physiological and

behavioral adaptations to survive there and applying this context to their enclosures and care

will help reduce disconnect between the natural and captive environments. For example,

understanding an animal's sensory experience and how it perceives the world should inform

both enclosure design and enrichment ideas (Newberry, 1995). Expanding upon Bartholomew’s

(1986) questions, Loughman (2020) has compiled a more robust questionnaire that allows for

detailed collection of natural history information, which serves as a great starting point for a

successful husbandry plan. The creation of species-specific care manuals that include this

information can increase the standard of care beyond the universal framework of welfare and

provide a singular resource for each species across various captive environments (Barber, 2009).

After evaluation at the species level, it is also important to consider that individuals of the same

species may interact with their exhibit or enrichment differently and these factors can have


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different impacts on an individual’s welfare (Soriano et al, 2006). Individuals may also have

different developmental factors and previous experiences to be considered (Newberry, 1995). In

the end, an effective husbandry plan must have clear goals and definitions of optimal welfare

(Browning, 2020) with ways to measure and assess the results of introducing enrichment and

enclosure changes on the welfare of the animals in question (Bennett et al., 2018; Loughman,

2020; Mellor, 2020).

Mason (2010) asserts that three traits can lend to vulnerability of a species adjusting sub-

optimally to captivity: species which (1) react with “flight”; (2) species with large home ranges or

migrations; and (3) species which are ecological specialists. The hypothesis suggests that over a

specific species’ evolutionary history the adaptations and behaviors present in the animal have

been optimized to maximize fitness in each environment (Kiley-Worthington, 1989). When there

is discord between one’s captive environment and its evolutionary history it may become

difficult for the organism to thrive since “hard-wired” physiological and psychological

adaptations and needs may be impossible to facilitate or engage. Although laboratory rats have

been domesticated for over a century and a half, they still exhibit a suite of behaviors from their

wild ancestor’s repertoire when placed in more naturalistic environments (Peplow, 2004).

Naturalistic designs have shown low frequencies of psychopathologies (Shidler and Boer, 1987;

Maple and Finlay, 1989; Kerridge, 1996; Maple and Perkins, 1996; Chang et al, 1999) and

facilitate normal behavioral patterns resembling wild-type activity budgets (Maple and Stine,

1982; Maple and Finlay, 1986; Ogden, 1990). Due to these trends, the biological relevance of any


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captive enclosure should be evaluated thoroughly for opportunities to improve this aspect of

welfare.

Differences Between Wild and Captive Populations of Animals

Long-term domestication of mice and rats has greatly shaped the behavioral patterns of

laboratory strains when compared to those of their wild ancestors (Gerlai, 2002; Holmes et al,

2002; Boice, 1981). Domestication has variously been associated with reduced levels of fear and

increased fertility (Huck and Price, 1975) as well as changes in defensive and cognitive social

behavior (Harker, 2002). The wild mouse has been reported to show high levels of aggressive

behavior and low levels of maternal care (Le Roy et al, 1998). On the contrary, inbred laboratory

mice engage in adult-directed interactions, olfactory investigations, and maternal behaviors

(Chalfin et al, 2014).

Captive wild rats were not found to form social hierarchies, they displayed more social

signals, maintained greater social distances, and they fought more fiercely than laboratory rats

(Boice, 1972; Barnett, 1963). Impoverished housing in rats and mice leads to impaired brain

development and heightened stress, respectively (Bennett et al, 1969; Renner and Rosenzweig,

1987; Sherwin and Olsson, 2004). The process of domestication in some cases seems to have

simply altered the expression of behaviors and genes. Burrows built by captive rats and mice are

often less complex than their wild counterparts (Stryjek et al, 2012). Ruan and Zhang (2015)

showed that domestication of mice and rats significantly altered the expression of oxytocin and

vasopressin in focal brain regions. Naturalistic housing conditions, on the other hand, were


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shown to predict a suite of neuroanatomical effects including improved cognition, visual-spatial

memory, and resistance to stress-induced pathology (Paylor et al, 1992; Faverjon et al, 2002;

Rockman et al, 1986).

Species of Interest for Improved Biological Relevance: The NM-R

To properly assess how to improve the enclosures of the College of Staten Island’s NM-R

colonies, we must first understand their natural history. This knowledge will shape the design

features, materials, and auxiliary systems surrounding the new housing system.

NM-Rs are one of six extant species in the Bathyergidae family, all of which are found on

the African continent. They can be found from the southernmost tip of Africa to mid-Ethiopia

and span diverse climatic zones, altitudes, and soils. However, most habitats in their range are

arid to semi-arid with sparse plant density and rainfall, and sandy to hard clay soils. Their

eusociality is rare among mammals (Faulkes and Bennett, 2013); with one breeding queen, a few

breeding males, and a colony of caste-segregated sterile members. Their behavior is more

analogous to bees and ants than it is to their fellow vertebrates. With the oldest known

individual reaching 37 years (Lewis & Buffenstein, 2016), they are also the longest-lived rodents

on the planet.

Depending on the number of individuals in a colony, which can range from roughly two

dozen to over two hundred, their underground burrows may encompass an area of a mile or

more and extend to depths of six feet (Brett 1991). These tunnels are constructed by a pair of

large ever-growing incisors which erupt in front of the animal’s lips. This is an adaptation which


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prevents the digging substrate from being inhaled by the animal (Buffenstein 2012). Almost

entirely subterranean, the air inside a burrow system would be difficult for other animals to

thrive in for long, with high humidity and oxygen concentrations sometimes falling below 15%

(Buffenstein, 2012). Chambers close to the surface are often used to gather and store food

whereas the deepest chambers are reserved for nesting. Within the vicinity of the nesting

chambers are separate pantry and toilet chambers. The toilet chambers serve an important role

in colony reproduction as it has been found that hormones in the queen's excrement are used to

suppress reproduction in other colony members and promote caring for her young. Pups are

brought into the toilet chambers soon after they are born to acquire this hormonal instruction as

well as the overall scent of the colony (Rozen, 2018). When the colony finds that the toilet

chamber is ‘full’, they will collapse the tunnel leading to it and excavate a new one.

As their name implies NM-Rs are nearly hairless, save for highly developed whiskers and a

series of hairs at evenly spaced intervals along their body. These hairs lend themselves to a

superior orienting response and highly developed somatosensory system. Hearing and vision are

much less developed than their sense of touch, proprioception, and smell, no doubt due to their

subterranean lifestyle (Buffenstein et al, 2012). A largely monomorphic species, colony members

have similar body weights, strength capacities, genitalia phenotype and anogenital distance.

Traits vary noticeably between three groups: breeding individuals, large workers, and small

workers (McCloskey, personal communications, July 2021); with the breeding female being the

largest member of the colony. Unlike most other mammals, NM-Rs depend on the environment

to regulate their body temperature. They will often move to different depths in the burrow to


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accomplish this but have also developed social behaviors like cuddling with other colony

members in a large pile to increase the heat of sleeping chambers.

In the wild, NM-Rs are sustained by a diet of bulbs, roots, tubers, and other geophytes.

They work in multiple small foraging platoons, dispersed across the colony to find scattered

food. Once found, foraging groups will carry back small bits to the nest, even going so far as to

‘farm’ the food sources by removing small chunks of the plant and then plugging it with soil so

that it may regenerate. Much like in insect colonies, food source locations are communicated

through odor trails and vocalizations (Judd and Sherman, 1996).

Design Features for the Improved Husbandry System

NM-R are relative newcomers to the laboratory environment, a mere 50-years,

compared to rats and mice who have been in the research scene since 1828 (Castle, 1947;

Gerlai, 2002) and 1926 (Frazer, 2007), respectively. While there is an abundance of works

centered on the biomedical potential of these odd rodents (Buffenstein et al, 2012; Delaney et

al, 2016), there is comparatively little in the way of housing and husbandry refinements;

meaning that even basic welfare studies, like those done for the rat in 1906 by the Wistar

Institute, are likely non-existent for the NM-R. Even when remarked upon, housing standards for

NM-Rs seem to stand in stark contrast to their natural habitats. NM-Rs are most often found in

hard solidified lateritic loam soil but have also been known to inhabit pure gypsum (Jarvis and

Sherman, 2002). However, they are often kept in captivity in wood shavings, corn cob, corn

husks, grasses, or paper towel in captivity (Wood and Mendez, 2002; Suckow, 2012; Chenlin et


NATURAL ENVIRONMENT

13

al, 2017). Some 30 years ago it was asserted that NM-R colonies bred in captivity continued to

resemble their wild counterparts (Brett, 1991; Jarvis 1981, 1991). Some studies suggest that this

may be changing, at least for related species. In studies with Cape mole-rats (Georychus

capensis), researchers found captive individuals to be behaviorally different from the wild

counterparts. Captive mole-rats were seen to interact differently with their environment,

showing decreased activity levels, slower responses to stimuli, and increased aggression

(Oosthuizen et al, 2013). Such information makes it imperative to heed the warning of the ills of

laboratory strain domestication and take a proactive approach to building evolutionarily relevant

enclosures for these organisms.

If we are to preserve their natural behavior for research, which is a priority for Dr.

McCloskey, then the housing must maintain as many of the known selective pressures as

possible to safeguard against the relaxation of their effects. A relevant enclosure would be made

of a substance which mimics the hard soils and rocks of the natural habitat. It would retain scent,

vital to the sensory and social world of the NM-Rs, and be able to hold humidity to allow the

colony to adjust the microclimate to their needs as they do in the wild. In the interest of the

animals’ welfare, the material used as a substrate would allow the NM-Rs to construct their own

tunnels and chambers as choice and control are imperative to positive animal welfare. As food

sparsity is thought to be a main driver of the rare eusociality seen in NM-Rs, an optimal housing

system would allow for the dispersed placement of food—something which does not happen

with current practices in our facility.


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Although meeting the needs of the target species is important, it is also necessary to ensure that

the design features of the new housing system offer an improvement in terms of occupational

safety for the animal care staff. Reducing the risk of injury due to repetitive motions induced by

the current housing system is critical. In addition, reducing the time spent on the husbandry

process would also be a huge boon to the efficiency of the modest staff. The reality of animal

research can be expensive for a small facility like CSI’s, and so it is also paramount that the

materials chosen are at least as affordable as the current system, if not more so.

The chronic ingestion of plastic has been shown to have a myriad of severe health effects

for many species including mice and rats (BANERJEE & SHELVER, 2021). Often, any chewing

behaviors directed at their plastic housing or enrichment is redirected towards safer chewing

options like wood or paper products, and implementation of stress-reduction protocols. While

other rodents may over-chew as a stress response, the fossorial NM-R has a natural imperative

to manipulate their environment in this way, be it to search for food, make room for an

expanding population, or restructure to adapt to changing weather conditions (Buffenstein

2012). Anecdotally, the NM-R colonies used in this study regularly chew on the plastic

connectors between each chamber - to the point of needing to have them replaced - despite

having ample access to raw tubers, hard commercial pellets, and paper enrichment. NM-Rs’

incisors grow through their lips to prevent excavated substrate from entering their mouths while

they dig (Park et al., 2010), so it is unlikely they would treat the plastic they try and tunnel

through as a food item, but it does not prevent the shredded plastic from adhering to their food

and being ingested unintentionally. Considering the wide range of deleterious effects plastic has


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on other rodents, even a small chance for chronic ingestion is reason enough to minimize plastic

in the new housing system in favor of a physiologically neutral material. In this same vein, the

material must be able to be disinfected or sterilized to reduce the introduction of harmful

pathogens to the system, and be hardy enough to not deteriorate, decompose or promote

microbial growth once in contact with the animals and their humid environment.

A Housing Substrate Candidate: Papercrete

Substrate candidates that could be used in the improvement of the housing system were

varied. Some were specifically made to be used around animals – such as compressed coconut

husk, excavator clay, and fluorite soil. These would be excellent options save for their cost and -

for the latter two products - weight. A cheaper earth-like product was Portland cement. Though

mixed on its own cement can be extremely heavy, when mixed with lighter materials such as

straw or even surfactant foam, it can become quite a bit lighter Since paper has been shown to

be safe with other rodents and the CSI NM-R colonies have had paper as nesting material for

years, it was assumed that paper would be a safe choice. Combining the two creates a light but

solidified material coined paper-concrete, or papercrete, for short. For this specific study,

newspaper was used due to easy accessibility and cost, though in practice any cellulose fiber like

straw or hemp may be used.


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Portland Cement

Portland cement is a generic term for a type of cement commonly found in concrete. One

may easily conflate cement and concrete due to their interchangeable use in the modern

vernacular, however, cement is technically referring specifically to the binding element within

concrete. When heated to approximately 1500 degrees Celsius, calcium silicate partially fuses to

become the binder called Portland cement. It is composed of finely ground and blended

limestone, calcium carbonate, and clay or shale (Advanced Concrete Technology, 2003).

Common concrete may contain between 10 to 15 percent cement, which mixes with

water to create a paste. That paste is then mixed with chosen aggregates, commonly stone or

gravel. The cement and water harden to bind these aggregates through hydration, and form a

rock-like mass which continues to strengthen as the concrete cures and ages (What’s the

Difference Between Cement and Concrete? 2015). The aggregates used with the cement can

change the fundamental structure and purpose of the finished project.

Portland cement is multifaceted and has multiple uses, some which show promise for the

purposes of this study. In 2009, a study suggested that Portland cement could be an alternative

to the more expensive mineral trioxide aggregate (MTA) used in dentistry for endodontic

procedures. Cured, or hardened, Portland cement is already a common component in fillings, is

non-toxic, and biocompatible (Hwang et al, 2009). Before it is cured, wet Portland cement and

dust do warrant some safety precautions and may be toxic (Adamu and Iloba, 2008), especially

to the skin and lungs as it contains trace amounts of heavy metals. Cured Portland cement is less

hazardous (OSHA). Therefore, it seems reasonable to assume that this material could be a safe


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choice for use with NM-Rs. Use of cured Portland cement with NM-Rs is not unprecedented. A

blog post by the Pacific Science Center dating back to 2009 stated that the facility would use

small blocks of pure Portland Cement as blockades for the animals to chew through (Something

to Chew On, 2009). Personal correspondence with the facility confirmed that they have utilized

Portland cement as enrichment since 1998 (S. Moore, personal communications, June 6, 2019).

Newspaper

Newspaper is composed of two ingredients: newsprint and ink. Newsprint is traditionally

made from mechanically and chemically processed wood pulp. Evergreens, softwoods, vegetable

fibers, and recycled paper products are ingredients commonly found in modern day newsprint.

The wood is chipped into small pieces and then steamed. Afterwards the ingredients are thermo-

chemically pulped and combined to form newspaper print. Newspaper ink is made by mixing a

vehicle solvent with a dye or pigment. Usually this solvent is linseed oil, soybean oil, or

petroleum distillate. The pigments added can be organic compounds like yellow lake or

phthalocyanine green, but also inorganics such as cadmium yellow or chrome green.

As CSI’s NM-R colonies have had positive experiences with pulped paper in the form of

paper towels, newspaper showed promise as a less expensive and more easily sourced option in

bulk. Much of the laboratory animal industry manufactures enrichment that is made of paper or

other fibrous materials. Examples include Nestlets, paper or pulp hides, and cardboard tubes.

(Hess et al, 2008; Bioe-Serv; Shepherd Specialty Papers). To help confirm their safety, Ochniewicz

et al (2019) studied heavy metal content in homemade and commercially available cardboard


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tubes, finding that neither type contained heavy metals, and that the only impurities in the two

were iron and copper– the levels of which were well lower than feeding standards for rodents.

Newspaper differs from the standard paper products used for laboratory animals in that

it includes ink. Although there are no studies to the author’s knowledge that evaluate ink toxicity

in NMRs, a reasonable comparison can be made with other species that do have such answers.

NMRs exhibit some of the highest digestive efficiency of all mammals, due in part to their

enlarged hindgut (Yahav and Buffenstein, 1992) as well as the highly efficient fermentation

process (Porter, 1957). Since they are strictly herbivores, with fermentative processes for

digestion and a large cecum, it seemed reasonable to consider other similarly equipped

mammals, such as ruminants, as proxies for judging NM-R safety in this scenario. Articles ranging

as far back as the early 1960s describe investigations into effects of dietary supplementation

with newspaper in cattle and sheep with no deleterious effects found(Mertens et al, 2019; Finn

et al, 2019; Wolf et al, 1994). Aderibigbe and Church (1987) showed that cardboard fiber was

more readily digested by growing lambs than that of ryegrass straw, confirming the potential for

effective utilization of the materials by the gut microorganisms. Considering this, newspaper was

deemed an acceptable material for this papercrete trial, but other options may still be evaluated

in the future.

Specific Aims

This study will investigate the viability of papercrete as a material for an improved

housing system for colonies of NM-Rs in a laboratory setting. Samples of the material will be


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created by hand and placed into the current housing system to be monitored for deterioration

and degradation over time. Indirect measures of wear and tear on sample blocks as well as

behavioral observations via video recordings will evaluate whether the NM-Rs treat the material

as a food or non-food item.

Methods

Subjects and Facilities

Two colonies of NM-Rs housed at the College of Staten Island will participate in this

study. Individual animals do not have names, instead the overall colony is named. For this study

colonies Linus and Terrific will be used.

The Terrific colony is an 11-member colony established in 2004. There is one breeding

female but at the time of writing this it has been roughly three years since she has birthed a

litter. The population at the time of the last litter was approximately 35 members and has since

then decreased to the current plateau of 11.

The Linus colony is the newest, established in March 2018 with 12 members at the time

of the investigation. There is one breeding female who has had two litters since colony

formation, though many members of the colony have since died. Colony members have had

intermittent issues with dry skin.


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Housing

All NM-R colonies are housed in an artificial burrow system comprised of square and

rectangular polycarbonate steam pans with fitted lids, connected by 5 cm inner diameter

polycarbonate tubes. Two heavy rocks are placed on top of each lid to prevent the colony

members from escaping; they have been known to pile substrate up against the walls to form a

ramp and push the lids out of the way if any less weight is used. Generally, the footprint of a

colony is increased as the colony population increases; at a rate of one chamber for every

additional 5-10 individuals, with a minimum of 2 chambers for a breeding pair. If a population

decreases overtime, the animal care staff does not usually reduce the number of chambers to

match.

Figure 1

Examples of Modular Caging System


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Colonies are maintained in temperature- and humidity-controlled rooms, at 29.2 ± 1.4° C

and ~20 % respectively, with extra heating supplied by reptile heat cables placed underneath the

chambers. Lighting is kept on a 12:12 hour lowlight: dark cycle; photos were taken in temporary

bright light for clarity.

Figure 2

NM-R Standing on Cob Substrate

A combination of cob material and shredded brown paper is used as bedding at the

bottom of each chamber, except for the chambers which the NM-Rs choose as their toilet, which

is left bare. This bedding is initially an inch deep in each chamber when freshly prepared but is

regularly redistributed by the colony.

A diet of tubers, squash, fruit, and Tekland Global 2019 laboratory chow are fed ad

libitum and refreshed on Mondays, Wednesdays, and Fridays. The presentation of the food is up

to the technician assigned to the animals, but generally vegetables are presented whole or cut


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into large chunks for the animals to chew through. All food is placed in the same chamber each

feeding; usually an end cap chamber.

Terrific has a total of 15 chambers and 23 tunnels that make up the enclosure, including a

feeding chamber (where food is placed by technicians) at the leftmost end, and two toilet

chambers of different sizes roughly in the middle of the layout (Figure 3). The Linus colony

enclosure has a total of 4 chambers and 4 tunnels, the rightmost chamber being the designated

food chamber and the leftmost the toilet chamber (Figure 4).

Figure 3

Layout of Chambers for Colony Terrific


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Figure 4

Layout of Chambers for Colony

Cleaning Routine

It takes about two full workdays to do a deep cleaning of each, which is done every 14

days. To start, all the mole-rats are taken out of the enclosure and placed in an empty holding

cage, ensuring the whole colony stays together. Then the technician works from one end of the

room to the other breaking down the caging. The PVC tubes connecting the chambers are

externally threaded and attached using internally threaded PVC couplers on the inside and

outside of each chamber. Once all the PVC components are disconnected the dirty bedding is

discarded and the chambers are scrubbed by hand to remove any stubborn excrement and

placed in an industrial washer on an acid sanitization cycle at 185℉. The PVC components are

loaded into large bins and soaked in a sanitizing solution of bleach (100ppm) for at least 8 hours,

usually overnight. They are then hand scrubbed and placed in a large brute can with drainage

holes drilled into the bottom. Once filled, the entire can is run through the same wash cycle as

the chambers to thoroughly rinse off the bleach solution, and then left to air-dry.

Materials

Papercrete Construction


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Manufacturing papercrete is a multistep process that takes nearly a month from start to

finish. The first step in the process was to shred newspaper and soak it in water for 24-48 hours.

The paper-water mixture was then pulped with a stucco paddle until the consistency was that of

porridge. This mixture was poured into cheesecloth and wrung out until it was no longer dripping

wet and could hold its shape when compressed. Portland cement was added next at a 2:1 ratio

of paper pulp to cement. According to the Portland Cement Association, a typical concrete

mixture - which is a mixture of water, cement, and rock aggregate - has a water content of 14-

21%. Other sources, such as Somayaji (2001) suggest that water content should be about 30%,

or 45-48% according to the NPCA Quality Control Manual for Precast Products. With the above

standards, we chose to add additional water amounting to 40% of the total mixture weight. This

was mixed by hand and then loaded into a silicone ice cube mold and left to set for 24 hours

covered with a trash bag to promote slow, even curing. After the initial 24-hour period, the

blocks were de-molded and set on a rack for further drying. The blocks were left to cure for a

total of 28 days, as is a standard cure time in the construction industry (Kosmatka & Wilson,

2017)


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Figure Error! Bookmark not defined.

Soaking and Mixing of Shredded Newspaper in a Process Known as "Pulping”

Figure 5

Papercrete Molding and Casting

Data Collection

It was important to ensure that the blocks could last just as long, if not longer than the

normal colony cleaning interval of 14 days, since it would be counterproductive to create a

substrate that would need to be changed even more frequently. This is both a convenience to


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the technicians as well as an effort to reduce disruption of the colonies as much as possible. This

test also served as an indirect measure of interaction with the blocks by the NM-Rs.

Before being placed in the chamber the blocks were weighed on a digital scale. The

initials of the colony name were written with non-toxic markers on all faces of the block and then

photographed all sides. When added to the colonies, the furthest location (Figure 7) from the

food chamber was chosen to reduce the chance of the blocks being confused with food Toilet

chambers were also intentionally avoided to prevent harmful pathogen growth and accelerated

maceration of the block. Blocks were placed in the center of the chosen testing chamber. Each

day the location of the blocks was noted, blocks were removed from the enclosure and gently

cleaned of debris such as cob or feces, visually inspected for mold or fungus growth and bite or

scratch marks, and then weighed. All sides of the block were photographed, and all colony initials

were refreshed if needed. The blocks were monitored in this way for a 14-day period or until the

block seemed too soiled to remain in the chamber with the animals.


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Figure 7

Testing Chamber Locations

Note. Diagram of Linus (left) and Terrific (right) colony layout with grey areas used to represent

placement of experimental blocks

Behavioral Observations Method

Video recordings of colony behavior were taken in the same chamber pre- and post-

introduction of the block using a GoPro 5. Two pre-block recordings were taken for each colony,

as well as two post-block recordings for each colony, totaling eight videos in all. Each recording

lasted 1 hour and 40 minutes for a total of 13 hours and 20 minutes of footage. These videos

were then examined using the program Loopy (Hofbauer & Stowers), which allows for time-

stamped behavioral data collection. The metrics measured during the video examination were

the number of individuals in the chamber, and the amount of time individuals spent in the


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chamber - or “duration of stay”. An individual was considered “in-chamber” under the following

conditions: (1) the entire individual was in the chamber, (2) the individual’s head and front paws

were in the chamber, or (3) the individuals head was in the chamber and engaged with either

the block, caging, or another colony member. Individuals considered “out-chamber” were those

with only their hind half in the chamber, or not present in the chamber at all.

To ensure reliability of observations, an extra observer was trained on two test

recordings: one with a single food item in the chamber (an analog for the experimental block)

and one without. Once comfortable with the training, the extra observer picked a random subset

of 4 videos (out of 8 total) to score using Loopy. The resulting data was then used to calculate

the Mean Duration per Occurrence of Inter-observer Agreement (IOA) with the given formula,

where Dur IOA is the Inter-observer Agreement percentage for each occurrence and n is the

number of occurrences:

Mean Duration Per Occurrence IOA %=Dur IOA1+Dur IOA2+Dur IOAn

n⋅ 100

Data Analysis

For comparisons of duration of stay in the testing chamber between treatments, t-tests

will be applied. Z-tests of independence will be used to assess if the categorical data of “in-

chamber” vs. “out-chamber'' are independent of treatment. ANOVAs will be used to look for

possible differences in how the NM-Rs populate the testing chamber when a block is present

versus when it is not. To look at the density trends further, a Spearman's rank correlation will be

used to investigate how the duration of stay in the testing chamber differs between treatments.


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Results

Papercrete Durability Test

The papercrete block was left with the Linus colony for a total of 15 days. Interestingly,

the block lost weight until day 11, where it began to gain weight until the block was removed on

day 15 (Figure 8). The block was weighed again after another week outside of the chamber

revealing a loss of 9 grams. We suspect this is due to the block being porous and absorbing

water. The weight at the beginning of the observation period was 86 grams, and after being

removed and left to dry for an additional week its final weight was 63 grams, for a total of 23

grams of material lost or 26.74% loss of weight.

Figure 8

Block Weight Over Time – Linus


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Figure 9

Test Block Day 1 vs. Day 15 – Linus

After the 15 days spent in the Linus colony, the block was removed of all straight edges

carved into more of an irregular sphere (Figure 9). The peaks of the material appeared dark

reddish-brown, like the color of fecal matter produced by the animals. The material did not have

a foul order nor any gross evidence of microbial growth.

The block left in Terrific colony began at 88 grams and was removed at 84 grams for a

total of 4 grams lost during the 14-day period (Figure 10), or a 4.76% loss of material. After two

weeks in contact with the NM-Rs, the Terrific block maintained most of its shape (Figure 11).

Teeth marks were most apparent where the lettering TER appears as some of the ink was

chewed off the block. The paper fibers can be seen more prominently in the after photo, as

opposed to the smooth surface in its original condition.


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Figure 10

Block Weight Over Time – Terrific

Figure 11

Test Block Day 1 vs. Day 15 – Terrific


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Behavioral Data

Inter-observer agreement for the behavioral coding was calculated using mean duration

per occurrence, resulting in observer agreement 87.15% of the time. Results for the Terrific

colony were based on only one individual ever being recorded as having visited the testing

chamber, therefore, limited statistical investigations could be performed.

To begin, the colonies data were compared to one another to determine if there were

differences in their interaction with the block. A two-sample Welch’s t-test assuming unequal

variances was performed to assess if the time spent in the testing chamber varied between the

colonies. Based on the data (Figure 12) the average duration of stay within the testing chamber

(MLinus= 63.35, SDLinus= 9.014; MTerrific= 62.307, SDTerrific=13.858) did not differ significantly

between colonies, regardless of treatment. Another two-sample Welch’s t-test assuming

unequal variances was performed to determine if the time spent in the testing chamber varied

between the two treatments; the block being present versus the block being absent. Based on

the data (Figure 13) the average duration of stay within the testing chamber with the block

present (MLinus= 68.456, SDLinus= 13.473; MTerrific= 52.635, SDTerrific= 13.6), did not differ

significantly between colonies. A final two-sample Welch’s t-test assuming unequal variances

was performed to assess if the time spent outside the testing chamber varied between colonies.

The data showed (Figure 14) the average duration of time outside the testing chamber (MLinus=

63.35, SDLinus= 9.014; MTerrific= 62.307, SDTerrific=13.858), did differ significantly between colonies

(p <0.001).


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Figure 12

Duration Inside Test Chamber Regardless of Treatment by Colony

Figure 6

Average Duration Inside Test Chamber With Block by Colony


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Figure 14

Average Duration Inside Test Chamber With Block by Colony

Next, the data for each colony was evaluated separately, beginning with the Linus colony.

A z- test of independence (x2 squared test) was performed to examine the relation between the

Linus colony’s location in reference to the testing chamber and the treatment type. The data

(Figure 15) shows these two variables to be independent of one another and non-significant (z =

0.485, p= 0.628). A two-sample Welch’s t-test assuming unequal variances was also performed

for this data (Figure 16), which found that the average duration of stay within the testing

chamber with the block present (M= 97.555, SD= 17.298), did not differ significantly from the

duration of stay when the block was not present (M= 107.137, SD= 17.71).

ANOVAs were performed to evaluate if the number of Linus members in the testing

chamber affected how long each member remained in the chamber when the block was present

(Figure 17), as well as when the block was not present (Figure 18). The average duration of stay

within the testing chamber with the block differed significantly when the testing chamber was


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populated with one NM-R (M = 27.711, SD= 3.566), two NM-Rs (M= 15.034, SD= 2.889), three

NM-Rs (M= 9.409, SD= 1.583) or four or more NM-Rs (M= 7.808, SD= 1.833). On the other hand,

the average duration of stay within the testing chamber without the block did not differ

significantly when the testing chamber was populated with one NMR (M = 28.969, SD= 5.017),

two NMRs (M= 21.588, SD= 4.57), three NMRs (M= 27.004, SD= 6.99) or four or more NMRs (M=

24.928, SD= 14.948). Based on the significant finding of the first ANOVA, a Spearmen’s rank

correlation was performed (Figure 19) which revealed a negative correlation between the

duration of time spent in the testing chamber and the number of NM-Rs present (r (218) = -

0.239, p < 0.001). In other words, the more NM-Rs were in the testing chamber with the block,

the shorter their stay.

Figure 15

Percent of Observed Location by Treatment – Linus


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Figure 16

Average Duration Inside Test Chamber by Treatment – Linus

Figure 17

Average Duration Inside Test Chamber With Block by Crowding Density – Linus


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Figure 18

Average Duration Inside Test Chamber Without Block by Crowding Density – Linus

Figure 19

Duration Inside Chamber With Block by Crowding Density – Linus


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The Terrific colony data was examined next. A z- test of independence was performed

first to examine the relation between the Terrific colony’s location in reference to the testing

chamber and the treatment type (Figure 20). These two variables were found to be independent

of one another and therefore non-significant; z = 0.643, p= 0.520. Next, a two-sample Welch’s t-

test assuming unequal variances was performed to determine if the duration of stay differed

between block treatments (Figure 21). The average duration of stay within the testing chamber

with the block present (M= 52.635, SD= 13.6), did not differ significantly from the duration of

stay when the block was not present (M= 81.649 1, SD= 31.881). Statistical investigations into

the number of occupants by treatment could not be performed for the Terrific colony because

only one NM-R was ever observed in the chamber during testing sessions.

Figure 20

Percent of Observed Location by Treatment – Terrific


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Figure 21

Average Duration Inside Test Chamber by Treatment - Terrific

Discussion

In the wild, NM-Rs are most often found in hard solidified lateritic loam soil but have

also been known to inhabit pure gypsum (Jarvis and Sherman, 2002) in colonies which can span

hundreds of feet (Buffenstein et al, 2012). This contrasts with captivity, where most of the time

guidelines suggest keeping the animals in wood shavings, corn cob, corn husks, grasses, or

paper towel (Wood and Mendez, 2002; Suckow, 2012; Chenlin et al, 2017). To our knowledge,

no other investigations exist which have attempted to increase the capacity for which a captive

enclosure more closely simulates the native habitat of NM-Rs. Therefore, much of the goal of

this study was to find ways to preserve as many selective pressures as possible which led to the

adaptations the NM-Rs are being studied for.


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Many of their adaptations allow them to thrive in arid and otherwise harsh

environments. NM-R food of choice are geophytes, which encompasses any plant that has an

enlarged storage system for storing nutrients and preventing water loss - usually by means of a

thick waxy coating or having a tough skin. These plants are usually adapted for semi-arid or

drought-ridden, harsh biomes renowned for poor soil quality (Howard et al 2019). It is no

wonder, then, that when studied it was found that NM-Rs have a relative bite force comparable

to that of Tasmanian devils - organisms which easily bite through femurs of much larger animals

(Hite et al. 2019). To enable such abilities, approximately 25% of the NM-Rs weight lies in their

jaw muscles (Sherman et. al. 1992). Those muscles also come in handy when building

underground burrows which can extend for up to a mile and have a depth of 2 meters

(Buffenstein 2012). Thus, these animals should be provided with ample chance to use their jaw

muscles if caretakers and researchers intend to maintain their current evolutionary history.

Contrary to that point, however, some of the most recent research published aimed to

“domesticate” NM-Rs with fixed cleaning and feeding times whilst keeping them in wood-

shavings (Yu et. Al 2017). This stands in stark contrast not only to their native biome, but also to

the leading theory of why their unique social structure evolved - the sparsity of food and other

resources in their environment. It seems fair to assume that much of the field has paused

research into methods of mimicking the “hard and impenetrable” (Buffenstein 2012) soils of the

NM-Rs home range or the chance to engage a large portion of their body weight in exercise. This

pause is risky, as genetic adaptation to captivity has been demonstrated to occur in as little as

one generation in other captive species (Christie et al. 2012).


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Papercrete Construction

The largest downside to using papercrete was the dust produced both in the making of

the material and when it was cut or gnawed into. This brought into question whether our mix

ratios did not allow for all the Portland cement to hydrolyze and harden completely or if this was

something of a normal behavior for the material. Utilization of Portland cement also required the

donning of masks, gloves, and protective eyewear to prevent injury due to its abrasive, caustic,

and absorbent characteristics. It also contains trace amounts of hexavalent chromium - a known

carcinogenic (OSHA 2008; National Toxicology Program 2021).

Another issue with the material was that it took approximately 28 days for the material to

initially cure and dry enough to be utilized. The process of curing in the construction industry is

usually hastened by use of accelerant compounds, but these were not considered for inclusion in

the current recipe for fear that the accelerants would pose even greater health risk to the

animals.

The other major component, newspaper, was found to be an excellent fiber for making

papercrete. The paper readily disintegrated after a 24-hour soak in water. Once blended, the

pulp mixture achieved the “porridge” consistency that repeatedly came across as a standard on

many of the DIY blogs. The only issue with creating the pulp was in the equipment used to blend

the mixture. For this preliminary investigation a Ryobi drill with a stucco mixing paddle

attachment was used. The drill was a one-handed trigger system that, after a few minutes of

holding, began to be painful. Future experiments will evaluate the usefulness of two-handed


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mortar mixers, or possibly a blender that can be left on without constant engagement, as one of

the primary aims of the study is to alleviate the risk of ergonomic injury in the husbandry

routine.

Lack of outdoor space in the facility meant that the process to manufacture papercrete

had to be slowed down to maintain cleanliness and organization with the materials as they

proved difficult to remove from surfaces once dried. This may prove to be a hindrance to

upscaling the project in this particular facility.

Once cured, the material was what one would expect of hardened concrete or cement.

The blocks were hard to the touch with very little give but also extremely light. The author found

the tactility of the papercrete to be reminiscent of plaster, the main ingredient of which is

gypsum, the raw material that NM-Rs inhabit in the wild (Jarvis and Sherman, 2002). Despite this

encouraging comparison, the health risk factors of Portland cement, combined with its long cure

time, and the nuisance of the dust generated by the manufacturing process have made it an

unfavorable material for future experiments.

Microclimate Efficacy

Leaving the blocks in the chambers with the NM-R for at least 14 days to investigate the

material’s durability proved successful. Both blocks were still intact, save for the rounding of the

edges by Linus colony. Neither of the blocks had any gross evidence of mold growth, foul odor,

or decay. In fact, the block placed in the Linus colony was stained with excrement and still did

not show signs of mold or pathogen growth. Pathogenic mold growth on concrete is associated


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43

with contact with moisture and is increased when the surface is soiled or allowed to collect dust

(Kiledal 2021; Viitanen & Ojanen 2007). While the absence of visible mold or bacterial film does

not preclude pathogenic presence on the papercrete blocks, lack of visible sporangiophores, or

the visible spore-containing stalks of mold/fungi, is a sign that the mold is at least non-

reproducing.

Weight was tracked for each block over the testing period as both a way to quantify

potential degradation and mold growth, such as swelling due to being in a humid environment,

but also as an indirect measure of interaction between the mole rats and the block. Comparing

the two colonies quantitatively and visually, the Linus colony rounded the edges of the blocks

into a sphere-like shape while Terrific only managed to graze off the ink marks on their block.

This is supported by the fact that Terrific only lost 4 grams of weight while Linus lost over 10

grams within the 14-day period. It was interesting to note that while the block from Terrific did

not change weight after being removed from the colony, the block from Linus colony continued

to lose another 9 grams from the final weight of 72 grams once removed, showing that the block

did indeed retain some amount of moisture. It remains to be seen if over a longer period this

water retention poses a threat to the health of the NM-Rs by promoting pathogen growth or

compromises the integrity of the papercrete matrix, however, the retention of moisture to some

degree may be beneficial as the NM-Rs seem to prefer high humidity environments.

In all, this assessment showed that papercrete could be successfully gnawed upon - a key

design feature. This lends well to papercrete being a material which could be altered by the NM-


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Rs at will, allowing the organisms to dictate their own colony infrastructure if given a large

enough volume of cured papercrete.

Behavioral Assessment

Behavioral investigations for this study were limited due to several factors. Normally the

animals are tracked using an RFID system and network analysis, so one does not need to have a

crystal-clear view on the animals to perform research on them. Due to this, high resolution

visuals were never a concern when setting up the current housing system, therefore the caging

is not entirely transparent. This meant that the “ethogram” for the animals was reduced to

looking at whether the animal was present in the testing chamber or not. While some of the

recordings offered the ability to see specific behaviors such as clawing or biting, the quality was

too inconsistent across the board to use those behaviors for any kind of statistical investigation.

Due to the NM-Rs preference of high humidity, many times even the reduced ethogram could

not be used as the droplets of condensation, wet food, or excrement blocked the view of the

camera.

The above limitations meant that many of the videos which were recorded were

unusable. This problem was only discovered once preliminary analysis of the first batches of

videos were started in February of 2020. While we had planned on recording new material,

many of the COVID-19 pandemic protocols had begun to take effect, which included stopping all

research on the NM-Rs until it was deemed safe again. By that time, it had already been decided


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that we would no longer go forward with our investigations into papercrete due to its dustiness,

thus the behavioral investigations discussed here are limited.

Though the Terrific and Linus colonies had different sized housing, and were separated in

age by approximately a decade, it was interesting to see that there was no significant difference

found in the duration of time spent within a testing chamber between the two. In Figure 17 the

differences between colonies were looked at regardless of treatment and in Figure 18 the t-test

performed only looked at the duration of time spent within the chamber with the block present.

The Terrific colony possessed more than three times the amount of housing space than Linus yet

they both had at least one individual present in the chamber.

Statistical testing for Linus showed that during the sessions without a block present,

there was no correlation found between the number of occupants and how long they spent in

the chamber. However, when a block was present, there was a strong negative correlation. This

meant that the more occupants present in the chamber, the less time each individual spent in

the chamber. The most likely cause of this is that within the Linus colony, the only place to put

the papercrete block was in a chamber which sat adjacent to the toilet chamber, making the

testing chamber an unintentional thruway. However, NM-Rs are known to form small foraging

and exploratory platoons after a new food source or item of interest is introduced to the colony.

It would be interesting to investigate if the negative correlation seen was due to the proximity to

other important chambers or related to exploratory behaviors. The Terrific colony had a much

larger colony footprint than Linus, so our choices of block placement were more varied in the

former. During recording sessions, the block was only ever visited by one NM-R in colony Terrific


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while in colony Linus there were frequently 4 or more individuals within the testing chamber.

Lack of multiple organisms in the chamber during recording sessions combined with

comparatively little degradation of the papercrete block would suggest that the Terrific colony

NM-Rs either did not see the block as something of interest to interact with or that the high

interaction rate by Linus members was due to the testing chamber’s position as a throughway.

It may also be the case that the metrics of duration and occupancy are ill-suited to

understanding the novelty of an object, its ability to mimic a substrate, and/or its worth to the

colony. Previously, it was thought that NM-Rs have discreet castes, with morphologic differences

amongst conspecifics to confer specialized abilities for specific tasks. However, research has

shown that whilst there exist such differences between reproductive members, dispersing

animals, and non-breeding animals, the specialization within non-breeding animals appears

more loosely defined (Buffenstein et al 2021). A study in 2016 found differential response to

oxytocin between members more frequently involved in colony defense and those less involved

(Hathaway et al 2016). It is possible that only certain members of a colony would ever visit or

interact with a novel substrate or object if they are each given distinct roles. If there are indeed

individuals who are designated soldiers or defenders, it may be their prerogative to ignore

inanimate objects that do not pose a clear threat to the colony. Therefore, it may be more

important to ask who exactly is frequenting the chambers and what is their role in the colony, as

well as testing if the responses differ with the blocks placed in differing locations within the

colony.


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Braude et. al (2021) remark that researchers must be wary of the interpretations of

colony social structure in extremely artificial captive settings. They imply that such settings may

inherently preclude high integrity interpretations. Therefore, studies focused on increasing

biological relevance may help unravel the complexities of role specialization within NM-R society.

Another aspect to consider is that interacting with the blocks may not be perceived as

beneficial to the NM-Rs in terms of energy conservation or infrastructure maintenance and

improvement. The NM-Rs are often seen trying to chew through the walls of the chambers they

are housed in. This behavior is not unexpected as it harkens back to their natural ecology as a

possible attempt at expansion. The blocks placed in the center of the caging, therefore, are not

obstacles to chew through which will allow access to a different chamber or expansion of the

colony since they can easily be moved to the side or walked around. Filling entire tunnels or

chambers with papercrete may evoke a differing response as the material may then be

energetically worth interacting with to allow for the animals to expand their housing of their own

volition, something which is critically lacking in captive environments, as Poole (1991) points out.

While the behavioral results are inconclusive, they prompt a wealth of further questioning and

help to structure more well-designed investigations for the future.


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References

Adamu, K., & Audu Sambo, B. (2008). Haematological Assessment of the Nile Tilapia Oreochromis

niloticus Exposed to Sublethal Concentrations of Portland Cement Powder in Solution.

International Journal of Zoological Research, 4, 48–52. https://doi.org/10.3923/ijzr.2008.48.52

Aderibigbe, A. O., & Church, D. C. (1987). Evaluation of cardboard and dried poultry waste as feed

ingredients for ruminants. Animal Feed Science and Technology (Netherlands).

https://scholar.google.com/scholar_lookup?title=Evaluation+of+cardboard+and+dried+poultry+

waste+as+feed+ingredients+for+ruminants&author=Aderibigbe%2C+A.O.+%28Ife+Univ.%2C+Ile-

Ife%2C+Oyo+State+%28Nigeria%29.+Dept.+of+Animal+Science%29&publication_year=1987

Akinwumi, I. I., Olatunbosun, O. M., Olofinnade, O. M., & Awoyera, P. O. (2014). Structural Evaluation

of Lightweight Concrete Produced Using Waste Newspaper and Office Paper. Civil and

Environmental Research, 9.

American Cement Manufacturers. (2019). Cement & Concrete Basics FAQs.

https://www.cement.org/cement-concrete/cement-and-concrete-basics-faqs

Balcombe, J. P. (2006). Laboratory environments and rodents’ behavioural needs: A review.

Laboratory Animals, 40(3), 217–235. https://doi.org/10.1258/002367706777611488

Banerjee, A., & Shelver, W. L. (2021). Micro- and nanoplastic induced cellular toxicity in mammals: A

review. The Science of the Total Environment, 755(Pt 2), 142518.

https://doi.org/10.1016/j.scitotenv.2020.142518

Bennett, A. J., Bailoo, J. D., Dutton, M. B., Michel, G. F., & Pierre, P. J. (2018a). Psychological Science

Applied to Improve Captive Animal Care: A Model for Development of a Systematic, Evidence-

https://doi.org/10.3923/ijzr.2008.48.52

https://scholar.google.com/scholar_lookup?title=Evaluation+of+cardboard+and+dried+poultry+waste+as+feed+ingredients+for+ruminants&author=Aderibigbe%2C+A.O.+%28Ife+Univ.%2C+Ile-Ife%2C+Oyo+State+%28Nigeria%29.+Dept.+of+Animal+Science%29&publication_year=1987



https://www.cement.org/cement-concrete/cement-and-concrete-basics-faqs

https://doi.org/10.1258/002367706777611488

https://doi.org/10.1016/j.scitotenv.2020.142518


NATURAL ENVIRONMENT

49

Based Assessment Of Environmental Enrichment for Nonhuman Primates. PsyArXiv.

https://doi.org/10.31234/osf.io/79xky

Bennett, A. J., Bailoo, J. D., Dutton, M., Michel, G. F., & Pierre, P. J. (2018b). Psychological Science

Applied to Improve Captive Animal Care: A Model for Development of a Systematic, Evidence-

Based Assessment Of Environmental Enrichment for Nonhuman Primates [Preprint]. PsyArXiv.


Bio-Huts for Mice, Certified. (n.d.). Bio-Serv. Retrieved April 20, 2022, from https://www.bio-

serv.com/product/Bio_Huts.html

Braude, S., Holtze, S., Begall, S., Brenmoehl, J., Burda, H., Dammann, P., Marmol, D., Gorshkova, E.,

Henning, Y., Hoeflich, A., Höhn, A., Jung, T., Hamo, D., Sahm, A., Shebzukhov, Y., Šumbera, R.,

Miwa, S., Vyssokikh, M. Y., Zglinicki, T., … Hildebrandt, T. B. (2021). Surprisingly long survival of

premature conclusions about naked mole-rat biology. Biological Reviews, 96(2), 376–393.

https://doi.org/10.1111/brv.12660

Brett, R. A. (2017). 5. The Ecology of Naked Mole-Rat Colonies: Burrowing, Food, and Limiting Factors.

In 5. The Ecology of Naked Mole-Rat Colonies: Burrowing, Food, and Limiting Factors (pp. 137–

184). Princeton University Press. https://doi.org/10.1515/9781400887132-008

Browning, H. (2020). The natural behaviour debate: Two conceptions of animal welfare. 23.

Buffenstein, R., Amoroso, V., Andziak, B., Avdieiev, S., Azpurua, J., Barker, A., Bennett, N., Brieño-

Enríquez, M., Bronner, G., Coen, C., Delaney, M., Dengler-Crish, C., Edrey, Y., Faulkes, C., Frankel,

D., Friedlander, G., Gibney, P., Gorbunova, V., Hine, C., & Smith, E. (2021). The naked truth: A



https://www.bio-serv.com/product/Bio_Huts.html

https://www.bio-serv.com/product/Bio_Huts.html


https://doi.org/10.1515/9781400887132-008


NATURAL ENVIRONMENT

50

comprehensive clarification and classification of current ‘myths’ in naked mole-rat biology.

Biological Reviews, 97. https://doi.org/10.1111/brv.12791

Buffenstein, R., Park, T., Hanes, M., & Artwohl, J. E. (2012a). Naked Mole Rat. The Laboratory Rabbit,

Guinea Pig, Hamster, and Other Rodents, 1055–1074. https://doi.org/10.1016/B978-0-12-

380920-9.00045-6

Buffenstein, R., Park, T., Hanes, M., & Artwohl, J. E. (2012b). Naked Mole Rat. The Laboratory Rabbit,

Guinea Pig, Hamster, and Other Rodents, 1055–1074. https://doi.org/10.1016/B978-0-12-

380920-9.00045-6

Chang, T. R., Forthman, D. L., & Maple, T. L. (1999). Comparison of confined mandrill (Mandrillus

sphinx) behavior in traditional and “ecologically representative” exhibits. Zoo Biology, 18(3),

163–176. https://doi.org/10.1002/(SICI)1098-2361(1999)18:3<163::AID-ZOO1>3.0.CO;2-T

Christie, M. R., Marine, M. L., French, R. A., & Blouin, M. S. (2012). Genetic adaptation to captivity can

occur in a single generation. Proceedings of the National Academy of Sciences, 109(1), 238–242.

https://doi.org/10.1073/pnas.1111073109

Delaney, M. A., Ward, J. M., Walsh, T. F., Chinnadurai, S. K., Kerns, K., Kinsel, M. J., & Treuting, P. M.

(2016a). Initial Case Reports of Cancer in Naked Mole-rats ( Heterocephalus glaber ). Veterinary

Pathology, 53(3), 691–696. https://doi.org/10.1177/0300985816630796

Delaney, M. A., Ward, J. M., Walsh, T. F., Chinnadurai, S. K., Kerns, K., Kinsel, M. J., & Treuting, P. M.

(2016b). Initial Case Reports of Cancer in Naked Mole-rats (Heterocephalus glaber). Veterinary

Pathology, 53(3), 691–696. https://doi.org/10.1177/0300985816630796


https://doi.org/10.1016/B978-0-12-380920-9.00045-6

https://doi.org/10.1016/B978-0-12-380920-9.00045-6

https://doi.org/10.1016/B978-0-12-380920-9.00045-6

https://doi.org/10.1016/B978-0-12-380920-9.00045-6

https://doi.org/10.1002/(SICI)1098-2361(1999)18:3%3c163::AID-ZOO1%3e3.0.CO;2-T

https://doi.org/10.1073/pnas.1111073109

https://doi.org/10.1177/0300985816630796

https://doi.org/10.1177/0300985816630796


NATURAL ENVIRONMENT

51

Edwin G. Foulke. (2008). Preventing Skin Problems fromWorking with Portland Cement. Occupational

Safety and Health Administration.

Faulkes, C. G., & Bennett, N. C. (2001). Family values: Group dynamics and social control of

reproduction in African mole-rats. Trends in Ecology & Evolution, 16(4), 184–190.

https://doi.org/10.1016/S0169-5347(01)02116-4

Finn, N. A., Cherry, N. M., Muir, J. P., & Smith, W. B. (2019). 167 Livestock Literacy: Ensiling newspaper

as a renewable fiber source for ruminant animals. Journal of Animal Science, 97(Suppl 1), 56.

https://doi.org/10.1093/jas/skz053.126

Fraser, D. (2008). Understanding animal welfare. Acta Veterinaria Scandinavica, 50(1), S1.

https://doi.org/10.1186/1751-0147-50-S1-S1

Harrison, T. (2003). 4 - Concrete properties: Setting and hardening. In J. Newman & B. S. Choo (Eds.),

Advanced Concrete Technology (pp. 1–33). Butterworth-Heinemann.

https://doi.org/10.1016/B978-075065686-3/50251-2

Hathaway, G. A., Faykoo-Martinez, M., Peragine, D. E., Mooney, S. J., & Holmes, M. M. (2016).

Subcaste differences in neural activation suggest a prosocial role for oxytocin in eusocial naked

mole-rats. Hormones and Behavior, 79, 1–7. https://doi.org/10.1016/j.yhbeh.2015.12.001

Hess, S. E., Rohr, S., Dufour, B. D., Gaskill, B. N., Pajor, E. A., & Garner, J. P. (2008). Home

Improvement: C57BL/6J Mice Given More Naturalistic Nesting Materials Build Better Nests.

Journal of the American Association for Laboratory Animal Science, 47(6), 7.

https://doi.org/10.1016/S0169-5347(01)02116-4

https://doi.org/10.1093/jas/skz053.126

https://doi.org/10.1186/1751-0147-50-S1-S1

https://doi.org/10.1016/B978-075065686-3/50251-2

https://doi.org/10.1016/j.yhbeh.2015.12.001


NATURAL ENVIRONMENT

52

Hill, W. C. O., Porter, A., Bloom, R. T., Seago, J., & Southwick, M. D. (1957). Field and Laboratory

Studies on the Naked Mole Rat, Heterocephalus Glaber. Proceedings of the Zoological Society of

London, 128(4), 455–514. https://doi.org/10.1111/j.1096-3642.1957.tb00272.x

Himmler, S. M., Modlinska, K., Stryjek, R., Himmler, B. T., Pisula, W., & Pellis, S. M. (2014).

Domestication and diversification: A comparative analysis of the play fighting of the Brown

Norway, Sprague-Dawley, and Wistar laboratory strains of (Rattus norvegicus). Journal of

Comparative Psychology, 128(3), 318–327. https://doi.org/10.1037/a0036104

Hite, N. J., Germain, C., Cain, B. W., Sheldon, M., Perala, S. S. N., & Sarko, D. K. (2019). The Better to

Eat You With: Bite Force in the Naked Mole-Rat (Heterocephalus glaber) Is Stronger Than

Predicted Based on Body Size. Frontiers in Integrative Neuroscience, 13.

https://www.frontiersin.org/article/10.3389/fnint.2019.00070

Home—Shepherd Specialty Papers—Cage Bedding & Enrichment. (n.d.). Shepherd Specialty Papers.

Retrieved April 20, 2022, from https://www.ssponline.com/

Howard, C. C., Folk, R. A., Beaulieu, J. M., & Cellinese, N. (2019). The monocotyledonous

underground: Global climatic and phylogenetic patterns of geophyte diversity. American Journal

of Botany, 106(6), 850–863. https://doi.org/10.1002/ajb2.1289

Hwang, Y.-C., Lee, S.-H., Hwang, I.-N., Kang, I.-C., Kim, M.-S., Kim, S.-H., Son, H.-H., & Oh, W.-M.

(2009). Chemical composition, radiopacity, and biocompatibility of Portland cement with

bismuth oxide. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics,

107(3), e96-102. https://doi.org/10.1016/j.tripleo.2008.11.015

https://doi.org/10.1111/j.1096-3642.1957.tb00272.x

https://doi.org/10.1037/a0036104

https://www.frontiersin.org/article/10.3389/fnint.2019.00070

https://www.ssponline.com/

https://doi.org/10.1002/ajb2.1289

https://doi.org/10.1016/j.tripleo.2008.11.015


NATURAL ENVIRONMENT

53

Jarvis, J. U. M., & Sherman, P. W. (2002). Heterocephalus glaber. Mammalian Species, 706, 1–9.

https://doi.org/10.1644/0.706.1

Judd, T., & SHERMAN, P. (1996). Naked mole-rats recruit colony mates to food sources. Animal

Behaviour - ANIM BEHAV, 52, 957–969. https://doi.org/10.1006/anbe.1996.0244

Kerridge, F. J. (2005). Environmental enrichment to address behavioral differences between wild and

captive black-and-white ruffed lemurs (Varecia variegata). American Journal of Primatology,

66(1), 71–84. https://doi.org/10.1002/ajp.20128

Kiledal, E. A., Keffer, J. L., & Maresca, J. A. (2021). Bacterial Communities in Concrete Reflect Its

Composite Nature and Change with Weathering. MSystems, 6(3), e01153-20.

https://doi.org/10.1128/mSystems.01153-20

Kosmatka, S., & Wilson, M. (2011). Design and Control of Concrete Mixtures.

Loughman, Z. J. (2020). Utilization of Natural History Information in Evidence based Herpetoculture: A

Proposed Protocol and Case Study with Hydrodynastes gigas (False Water Cobra). Animals,

10(11), 2021. https://doi.org/10.3390/ani10112021

Maple, T. L., & Bloomsmith, M. A. (2018). Introduction: The science and practice of optimal animal

welfare. Behavioural Processes, 156, 1–2. https://doi.org/10.1016/j.beproc.2017.09.012

Maple, T. L., & Finlay, T. W. (1989). Applied primatology in the modern zoo. Zoo Biology, 8(S1), 101–

116. https://doi.org/10.1002/zoo.1430080511

Maple, T. L., & Perkins, L. A. (1996). Enclosure furnishings and structural environmental enrichment.

University of Chicago Press.

https://scholar.google.com/scholar_lookup?title=Enclosure+furnishings+and+structural+environ

https://doi.org/10.1644/0.706.1

https://doi.org/10.1006/anbe.1996.0244

https://doi.org/10.1002/ajp.20128

https://doi.org/10.1128/mSystems.01153-20

https://doi.org/10.3390/ani10112021

https://doi.org/10.1016/j.beproc.2017.09.012

https://doi.org/10.1002/zoo.1430080511

https://scholar.google.com/scholar_lookup?title=Enclosure+furnishings+and+structural+environmental+enrichment&author=Maple%2C+T.L.+%28Zoo+Atlanta%2C+Atlanta%2C+GA.%29&publication_year=1996


NATURAL ENVIRONMENT

54

mental+enrichment&author=Maple%2C+T.L.+%28Zoo+Atlanta%2C+Atlanta%2C+GA.%29&public

ation_year=1996

Mason, G. (2006). Stereotypic behaviour in captive animals: Fundamentals and implications for

welfare and beyond. In G. Mason & J. Rushen (Eds.), Stereotypic animal behaviour:

Fundamentals and applications to welfare (2nd ed., pp. 325–356). CABI.

https://doi.org/10.1079/9780851990040.0325

Mason, G., Burn, C. C., Dallaire, J. A., Kroshko, J., McDonald Kinkaid, H., & Jeschke, J. M. (2013). Plastic

animals in cages: Behavioural flexibility and responses to captivity. Animal Behaviour, 85(5),

1113–1126. https://doi.org/10.1016/j.anbehav.2013.02.002

Mason, G. J. (2010). Species differences in responses to captivity: Stress, welfare and the comparative

method. Trends in Ecology & Evolution, 25(12), 713–721.

https://doi.org/10.1016/j.tree.2010.08.011

Max Hofbauer & John Stowers. (n.d.). loopbio—About. Loopbio. Retrieved April 20, 2022, from

http://loopbio.com/about/

McCloskey, D. (2011, January 1). From market baskets to mole rats: Using data mining techniques to

analyze RFID data describing mole rat behavior. McCloskey Lab Webpage.

http://www.neuro.nyc/publication/2011-01-01_mccloskey20111/

Mellor, E. L. (2020). Does natural foraging niche influence captive animal health and welfare? 348.

Mertens, D. R., Campbell, J. R., Martz, F. A., & Hilderbrand, E. S. (1971). Lactational and Ruminal

Response of Dairy Cows to Ten and Twenty Percent Dietary Newspaper. Journal of Dairy Science,

54(5), 667–672. https://doi.org/10.3168/jds.S0022-0302(71)85904-0



https://doi.org/10.1079/9780851990040.0325

https://doi.org/10.1016/j.anbehav.2013.02.002

https://doi.org/10.1016/j.tree.2010.08.011

http://loopbio.com/about/

http://www.neuro.nyc/publication/2011-01-01_mccloskey20111/

https://doi.org/10.3168/jds.S0022-0302(71)85904-0


NATURAL ENVIRONMENT

55

National Toxicology Program. (2021). National Toxicology Program: 15th Report on Carcinogens.

National Toxicology Program (NTP). https://ntp.niehs.nih.gov/go/roc15

Newberry, R. C. (1995). Environmental enrichment: Increasing the biological relevance of captive

environments. Applied Animal Behaviour Science, 44(2–4), 229–243.

https://doi.org/10.1016/0168-1591(95)00616-Z

Newman, J., & Choo, B. S. (Eds.). (2003). Frontmatter. In Advanced Concrete Technology (pp. i–iii).

Butterworth-Heinemann. https://doi.org/10.1016/B978-0-7506-5686-3.50314-1

Ochniewicz, P., Garnuszek, P., Karczmarczyk, U., Laszuk, E., & Sochaczewski, Ł. (2019). Heavy metal

content in environmental enrichment used for laboratory rodents. Zeszyty Problemowe

Postępów Nauk Rolniczych, 597, 23–29. https://doi.org/10.22630/ZPPNR.2019.597.9

Ochniewicz, P., Karczmarczyk, U., Sochaczewski, L., Laszuk, E., & Garnuszek, P. (2019). Heavy metal

content in environmental enrichment used for laboratory rodents. Zeszyty Problemowe

Postępów Nauk Rolniczych, 597. https://doi.org/10.22630/ZPPNR.2019.597.9

Ogden, J. J., Finlay, T. W., & Maple, T. L. (1990). Gorilla adaptations to naturalistic environments. Zoo

Biology, 9(2), 107–121. https://doi.org/10.1002/zoo.1430090205

Olsson, I. A. S., Nevison, C. M., Patterson-Kane, E. G., Sherwin, C. M., Van de Weerd, H. A., & Würbel,

H. (2003). Understanding behaviour: The relevance of ethological approaches in laboratory

animal science. Applied Animal Behaviour Science, 81(3), 245–264.

https://doi.org/10.1016/S0168-1591(02)00285-X

https://ntp.niehs.nih.gov/go/roc15

https://doi.org/10.1016/0168-1591(95)00616-Z

https://doi.org/10.1016/B978-0-7506-5686-3.50314-1

https://doi.org/10.22630/ZPPNR.2019.597.9

https://doi.org/10.22630/ZPPNR.2019.597.9

https://doi.org/10.1002/zoo.1430090205

https://doi.org/10.1016/S0168-1591(02)00285-X


NATURAL ENVIRONMENT

56

Olsson, I. A. S., Nevison, C. M., Patterson-Kane, E. G., Sherwin, C. M., Weerd, H. A. V. de, & Würbel, H.

(2003). Understanding behaviour: The relevance of ethological approaches in laboratory animal

science. Applied Animal Behaviour Science, 3(81), 245–264.

Olsson, I., & Sherwin, C. (2004). Behavioural Activity of Laboratory Mice in Standard and Furnished

Cages with a Running Wheel. 38th International Congress of ISAE, Helsinki, Finland, 241–241.

Oosthuizen, M. K., Scheibler, A.-G., Charles Bennett, N., & Amrein, I. (2013). Effects of Laboratory

Housing on Exploratory Behaviour, Novelty Discrimination and Spatial Reference Memory in a

Subterranean, Solitary Rodent, the Cape Mole-Rat (Georychus capensis). PLoS ONE, 8(9),

e75863. https://doi.org/10.1371/journal.pone.0075863

Pacific Science Center Life Sciences: Something to Chew On. (2009, October 21). [Pacific Science

Center]. Pacific Science Center Life Sciences. http://pacscilife.blogspot.com/2009/10/something-

to-chew-on.html

Park, T. J., Lewin, G. R., & Buffenstein, R. (2010). Naked Mole Rats: Their Extraordinary Sensory World.

In M. D. Breed & J. Moore (Eds.), Encyclopedia of Animal Behavior (pp. 505–512). Academic

Press. https://doi.org/10.1016/B978-0-08-045337-8.00152-2

Peplow, M. (2004). Lab rats go wild in Oxfordshire. Nature. https://doi.org/10.1038/news040202-2

Poole, T. B. (1991). Criteria for the provision of captive environments. In H. O. Box (Ed.), Primate

Responses to Environmental Change (pp. 357–374). Springer Netherlands.

https://doi.org/10.1007/978-94-011-3110-0_19

https://doi.org/10.1371/journal.pone.0075863

http://pacscilife.blogspot.com/2009/10/something-to-chew-on.html


https://doi.org/10.1016/B978-0-08-045337-8.00152-2

https://doi.org/10.1038/news040202-2

https://doi.org/10.1007/978-94-011-3110-0_19


NATURAL ENVIRONMENT

57

Price, E. O. (1973). Some behavioral differences between wild and domestic Norway rats: Gnawing

and platform jumping. Animal Learning & Behavior, 1(4), 312–316.

https://doi.org/10.3758/BF03199259

Renner, M. J., & Rosenzweig, M. R. (1986). Social interactions among rats housed in grouped and

enriched conditions. Developmental Psychobiology, 19(4), 303–313.

https://doi.org/10.1002/dev.420190403

Rozen, D. E. (2018). Eating poop makes naked mole-rats motherly. The Journal of Experimental

Biology, 221(21), jeb170183. https://doi.org/10.1242/jeb.170183

Schilder, M. B. H., & Boer, P. L. (1987). Ethological investigations on a herd of plains zebra in a safari

park: Time-budgets, reproduction and food competition. Applied Animal Behaviour Science,

18(1), 45–56. https://doi.org/10.1016/0168-1591(87)90253-X

Sherman, P. W., & Jarvis, J. U. M. (2002). Extraordinary life spans of naked mole-rats ( Heterocephalus

glaber ). Journal of Zoology, 258(3), 307–311. https://doi.org/10.1017/S0952836902001437

Sheth, J. T., & Joshi, S. (2015). Paper Crete: A Sustainable Building Material. 6.

Somayaji, S. (2001). Civil engineering materials. Prentice Hall.

Soriano, A. I., Ensenyat, C., Serrat, S., & Maté, C. (2006). Introducing a Semi-Naturalistic Exhibit As

Structural Enrichment for Two Brown Bears (Ursus arctos). Does This Ensure Their Captive Well-

Being? Journal of Applied Animal Welfare Science, 9(4), 299–314.

https://doi.org/10.1207/s15327604jaws0904_5

Steve Ritter. (1998, November 16). WHAT’S THAT STUFF? - Ink.

https://pubsapp.acs.org/cen/whatstuff/stuff/7646scit2.html

https://doi.org/10.3758/BF03199259

https://doi.org/10.1002/dev.420190403

https://doi.org/10.1242/jeb.170183

https://doi.org/10.1016/0168-1591(87)90253-X

https://doi.org/10.1017/S0952836902001437

https://doi.org/10.1207/s15327604jaws0904_5

https://pubsapp.acs.org/cen/whatstuff/stuff/7646scit2.html


NATURAL ENVIRONMENT

58

Terry. (2009, October 21). Something to Chew On. Pacific Science Center Life Sciences.


Viitanen, H., & Ojanen, T. (2007). Improved Model to Predict Mold Growth in Building Materials. 8.

Wolf, B. W., Titgemeyer, E. C., Berger, L. L., & Fahey, G. C., Jr. (1994). Effects of chemically treated,

recycled newsprint on feed intake and nutrient digestibility by growing lambs. Journal of Animal

Science, 72(9), 2508–2517. https://doi.org/10.2527/1994.7292508x

Wood, D., & Mendez, R. (1991). HUSBANDRY STANDARDS FOR KEEPING NAKED_MOLE RATS IN

CAPTIVITY INTRODUCTION - PDF Free Download. https://docplayer.net/38146421-Husbandry-

standards-for-keeping-naked_mole-rats-in-captivity-introduction.html

Yahav, S., & Buffenstein, R. (1992). Caecal function provides the energy of fermentation without

liberating heat in the poikilothermic mammal, Heterocephalus glaber. Journal of Comparative

Physiology B, 162(3), 216–218. https://doi.org/10.1007/BF00357526

Yu, C., Wang, S., Yang, G., Zhao, S., Lin, L., Yang, W., Tang, Q., Sun, W., & Cui, S. (2017). Breeding and

Rearing Naked Mole-Rats (Heterocephalus glaber) under Laboratory Conditions. Journal of the

American Association for Laboratory Animal Science : JAALAS, 56(1), 98–101.

Zions, M., Meehan, E. F., Kress, M. E., Thevalingam, D., Jenkins, E. C., Kaila, K., Puskarjov, M., &

McCloskey, D. P. (2020). Nest Carbon Dioxide Masks GABA-Dependent Seizure Susceptibility in

the Naked Mole-Rat. Current Biology, 30(11), 2068-2077.e4.

https://doi.org/10.1016/j.cub.2020.03.071


https://doi.org/10.2527/1994.7292508x

https://docplayer.net/38146421-Husbandry-standards-for-keeping-naked_mole-rats-in-captivity-introduction.html

https://docplayer.net/38146421-Husbandry-standards-for-keeping-naked_mole-rats-in-captivity-introduction.html

https://doi.org/10.1007/BF00357526

https://doi.org/10.1016/j.cub.2020.03.071

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