Evidence that zoo visitors influence HPA activity in spider monkeys (Ateles geoffroyii rufiventris)

Evidence that zoo visitors influence HPA activity

in spider monkeys (Ateles geoffroyii rufiventris)

Nick Davisa,b,c,d,*, Colleen M. Schaffnera,c, Tessa E. Smithb,c

aDepartment of Psychology, University College Chester, Parkgate Road, Chester, CH1 4BJ, UKbDepartment of Biology, University College Chester, Parkgate Road, Chester, CH1 4BJ, UK

cChester Centre for Stress Research, University College Chester, Parkgate Road, Chester, CH1 4BJ, UKdZoological Gardens Chester, Upton-by-Chester, CH2 1LH, UK

Available online 13 November 2004

Abstract

There has been conflicting evidence about the impact of visitors on zoo animals. The present study

was designed to increase understanding of visitor effect by assessing the relationship between visitor

numbers and activity in the hypothalamic–pituitary–adrenal (HPA) axis. An enzyme-immunoassay

was successfully developed and validated to quantify urinary cortisol in spider monkeys. The

physiological impact of visitors on the monkeys was then investigated by assessing the levels of

urinary cortisol in samples collected when no visitors were in the zoo and throughout the year when

visitor density fluctuated widely. Our results suggest that an increase in the number of visitors was

associated with an increase in cortisol. This study supports previous behavioural research that visitors

have a meaningful impact on primates in zoos. It also increases our understanding of visitor effect by

assessing the relationship between absolute visitor numbers and an aspect of the animals’ physiology.

# 2004 Elsevier B.V. All rights reserved.

Keywords: Visitor effect; Urinary cortisol; Spider monkeys; Stress

1. Introduction

There has been conflicting evidence regarding the effect that visitors have on the lives of

captive animals. Some researchers have reported no effect of zoo visitors on animals

(Synder, 1975), whereas other researchers report enriching (Fa, 1989; Cook and Hosey,

www.elsevier.com/locate/applanim

Applied Animal Behaviour Science 90 (2005) 131–141

* Corresponding author.

E-mail address: [email protected] (N. Davis).

0168-1591/$ – see front matter # 2004 Elsevier B.V. All rights reserved.

doi:10.1016/j.applanim.2004.08.020

1995) or negative effects (Hediger, 1969; Chamove et al., 1988; Skyner et al., 2004). There

are many factors that could be influencing the impact of visitors on zoo animals’ well being

which have been outlined by Hosey (2000). Variables that could potentially influence the

visitor–captive animal relationships include inter-species variation (Chamove et al., 1988;

Clarke and Mason, 1988; Mitchell et al., 1992; Wormell et al., 1996), enclosure design

(Mitchell et al., 1990; Glatston et al., 1984; Chamove et al., 1988; Hosey, 2000; Carlstead

and Shepherdson, 2000) and visitor characteristics (Hosey and Druck, 1987; Mitchell et al.,

1991; Hosey, 2000; Birke, 2001). Although there is a general consensus that visitors can

have a negative impact on zoo animals, there is sufficient inconsistency to warrant further

study (Hosey, 2000). Previous studies exclusively relied on behavioural indices to assess

the impact of visitors on animals, and to our knowledge, only one previous study has used

physiological indices to assess visitor impact (Kalthoff et al., 2001). This study attempted

to increase our understanding of visitor effect by assessing the relationship between visitor

numbers and one aspect of an animal’s physiology; activity in the hypothalamic–pituitary–

adrenal (HPA) axis.

Previous studies have demonstrated that the analysis of urine and faeces can provide an

effective method of measuring reproductive steroid metabolites in Neotropical primates,

such as marmosets and tamarins (French et al., 1996; Smith et al., 1997; Ziegler and

Snowdon, 2000; Ziegler et al., 2000). Campbell et al. (2001) has used faecal analysis to

investigate levels of pregnane-diol 3a glucuronide and estrone conjugates in the ovarian

cycles in female black-handed spider monkeys (Ateles geoffroyi rufiventris).

Cortisol, another steroid hormone, is the end product of HPA activity and is an effective

marker for assessing physiological stress in captive animals (Ziegler et al., 1995; Smith and

French, 1997; Whitten et al., 1998; Boinski et al., 1999; Crockett et al., 2000). Therefore

measurement of cortisol in the urine can potentially provide information about the

physiological response of a non-human primate to a potential stressor, such as visitors.

In February 2001, foot and mouth disease (FMD) appeared in the UK with a

devastating impact on all livestock industries. Consequently, strict restrictions were

imposed on the movement and handling of animals throughout the country. Farms, zoos

and safari parks were closed to all but essential staff for the duration of the outbreak.

Chester Zoo was closed for a total of 6 weeks from 25 February 2001 to 6 April 2001.

During this time only essential keeping staff where allowed into the zoo. The closure of

Chester Zoo provided a unique opportunity to collect data for a period when there were

no zoo visitors.

The first aim of our study was to develop and validate an enzyme-immunoassay for the

measurement of urinary cortisol in black-faced spider monkeys (A. geoffroyii rufiventris,

Rylands et al., 2000). The immunological validation followed Diamandus and

Christopoulos (1996) suggestions for appropriate immunoassay protocols. The assay

was biologically validated by assessing whether the typical diurnal pattern of cortisol

excretion, evident in the plasma of many primate species (Clarke et al., 1996; Saltzman

et al., 1998; Gust et al., 2000; Abbott et al., 2003), could be detected in the urine.

The second aim of our study was to investigate the physiological impact of visitors on

the spider monkey HPA axis by quantifying levels of urinary cortisol in samples collected

during days of varying visitor numbers (i.e. 0–16,500 visitors). The relationship between

concentrations of urinary cortisol and actual visitor numbers were then investigated. We

N. Davis et al. / Applied Animal Behaviour Science 90 (2005) 131–141132

predicted that if visitors adversely impacted the animals then a positive relationship would

be identified between urinary cortisol and visitor numbers.

2. Method

2.1. Subjects and housing

The study involved four adult females, one adult male and two juvenile males from a

breeding group of Colombian spider monkeys (A. geoffroyii rufiventris) housed at Chester

Zoo. The animals were housed in an indoor enclosure measuring 11.5 m � 12 m � 5 m,

which was furnished with many ropes, logs, branches, hammocks and various enrichment

devices to encourage arboreal behaviour (Fig. 1a). The animals also had access to an

outside enclosure measuring 60 m � 55 m � 30 m, which contained trees, shrubs and 8 m

pine poles interconnected with ropes (Fig. 1b). The subjects had free access to both indoor

and outdoor enclosures throughout the year, except during cold periods when they did not

N. Davis et al. / Applied Animal Behaviour Science 90 (2005) 131–141 133

Fig. 1. Diagrammatic representations of the indoor (a) and outdoor (b) enclosures in which the subjects were

housed at Chester Zoo.

have night-time access to the outside enclosure. The indoor area was connected to the

outdoor area by two tunnels (3 m � 0.8 m � 0.8 m), which passed through a keeper area.

The animals were normally maintained as one group, however there was the potential to

separate animals at the back of the indoor enclosure when required (12 m � 2.5 m � 4 m).

Public viewing was achieved inside through four large viewing windows (2.4 m � 2.2 m)

and from the outside along two sides of the enclosure. The tunnels and vegetation provided

areas of privacy where the monkeys could escape from public view.

The bedding consisted of a deep litter floor covering of wood bark and was cleaned

daily. Typically the monkeys received three feeds each day. The morning feed consisted of

600 g of Primate pellets (Wildlife feeds, England) and a supplemented protein such as eggs

or mealworms. They were also fed fruit and vegetables two times each day at varying

times, supplemented with bread and Vionate vitamin and mineral powder (Sherley’s

Beaphar UK Ltd, Homefield Road, Haverhill, Suffolk, CB9 8QP, UK). Food was presented

in a variety of ways throughout the indoor and outdoor enclosure to encourage natural

arboreal feeding behaviour. Water was available ad libitum in the indoor and outdoor

enclosures.

2.2. Procedure

2.2.1. Urine collection

Urine collection was conducted three to four times a week between 07:00 and 08:00 h.

This coincided with the daily husbandry regime when the monkeys were vacated from their

inside enclosure. During this time the animals typically rested and waited in the tunnels

over the keeper area. Researchers were able to stand under the tunnels and collect urine in

aluminium trays without the requirement for any form of training. The samples were

immediately stored at �20 8C until assayed.

2.2.2. Cortisol assay validation

Levels of cortisol were measured in all urine samples using a modified enzyme-

immunoassay (EIA) applied previously by Smith and French (1997). Samples were diluted

1:256–1:512 as necessary and run in duplicate. Inter-assay coefficients of variation were

2.03% for the high pool and 11.51% for the low pool. Intra-assay coefficients of variation

were 5.67 and 4.40% for the high and low pools, respectively.

2.2.3. Creatinine assay

The hormone concentration for each sample was corrected for creatinine concentration

using a modified Jaffe end-point assay (Burtis and Ashwood, 2001) and samples diluted to

1:200. Inter- and intra-assay coefficients of variations were 11.47 and 2.16%, respectively.

2.2.4. Immunological validation

Immunological validation followed Diamandus and Christopoulos, (1996) suggestions

for appropriate immunoassay protocols demonstrating specificity, accuracy, precision and

sensitivity. Assay specificity was determined by using four displacement curves of halving

dilutions of a urine pool for seven spider monkeys to determine parallelism to cortisol

standards (one standard displacement curve was compared to two urine displacement


curves). Assay accuracy was determined by adding a low (1:2048), medium (1:1024) and a

high concentration (1:32) of pooled urine to six serial diluted standard samples [500, 250,

125, 62.5, 31.25, 15.12 pg/50 ul)] to ascertain sample recovery. Precision was ascertained

across all samples by monitoring inter- and intra-assay coefficient of variations.

2.2.5. Biological validation

The biological validation involved verifying the presence of diurnal variation in the

excretion of cortisol metabolites. Urinary cortisol is known to follow a diurnal pattern

whereby cortisol levels peak in the early morning when the animals awaken and then

gradually decreases throughout the day to reach a nadir when the animals retire (e.g.,

Crockett et al., 2000; Coe and Levine, 1995). The five adults contributed urine samples to

the circadian assessment. Samples were collected opportunistically from 08:00 to 18:00 h

for 3 days over a 7-day period from the five subjects.

2.2.6. Visitor study

The physiological impact of visitors on the monkeys was investigated by assessing

the levels of urinary cortisol. Samples were collected during the FMD outbreak when no

visitors were in the zoo and throughout the year when visitor density fluctuated widely.

This study used the total number of visitors in the zoo and related this to the

concentration of urinary cortisol in the sample collected the next morning to account for

a lag in the excretion of urinary cortisol (Whitten et al., 1998; Bahr et al., 2000). We

selected samples using the Chester Zoo records, notes from our urine file and diary notes

maintained by CMS. We only included samples when we were confident that no other

physical or social stressful events were occurring. We avoided any samples collected in

the 3 days following a social or physical stressor and samples that preceded a known

social conflict between animals. A previous study of marmosets revealed that cortisol

levels increase prior to the outbreak of serious conflict between animals (Smith and

French, 1997).

It must be noted that for the period 7 months before the FMD outbreak and throughout

the zoo closure, the breeding male had been separated from the rest of the group for animal

management reasons. Although isolated from the rest of the group he still had full visual

and also limited physical contact with the females and juveniles. He was reintroduced back

into the group 3 weeks after the zoo reopened. To ensure that this separation was not itself a

source of stress we used a matched paired t-test to compare the mean urinary cortisol values

for all members of the group during periods when the breeding male was separated and

after he had been reintroduced. Cortisol levels for the group did not vary significantly as a

function of the breeding male’s location in or out of the group (P = 0.143, d.f. = 4, S.E. =

0.824). This indicated that the separation did not confound the study.

2.3. Data analysis

To determine assay accuracy, regression analysis was performed to determine the extent

to which commercial standards were recovered in the urine pools. To assess specificity, the

F-statistic was used to compare the slopes of the linear regressions of the displacement

curves produced by the pooled monkey urine and commercial standards. To assess


circadian variation in urinary cortisol excretion during the day (08:00–18:00 h), we

divided the diurnal period into 5 time blocks: 08:00–09:59; 10:00–11:59; 12:00–13:59;

14:00–15:59 and 16:00–17:59 h. We collapsed the samples for each subject across

the three collection days. The mean concentration of urinary cortisol was calculated for

each animal in each time slot and the data were analysed using a one-factor repeated

measure analysis of variance. This test was followed by a linear trend analysis to determine

if there was a significant decreasing pattern over time of day (Keppel, 1993). We required

at least two samples from two different monkeys on a given day to assess whether

absolute visitor numbers were associated with urinary cortisol. A Spearman’s rank

correlation coefficient was performed to test for an association. We selected a non-

parametric test in this instance because the presence of 10 data points for visitor numbers at

0 led to a skewed distribution as revealed by a significant Kolmogorov–Smirnov test (Z =

1.62, N = 77, P = 0.01). To further explore the impact of visitors on HPA function we used a

repeated measures one-factor analysis of variance (ANOVA) to compare cortisol levels

across 4 categories of daily visitor numbers. These were zero (no visitors), low (1–999),

medium (1000–6999) and high (>7000) and were based on historic visitor data. When

relevant, we assumed a two-tailed distribution and adopted an a level of 0.05 for all

statistical tests.

3. Results

3.1. Immunological validation

The four serial dilutions of pooled spider monkey urine produced displacement curves

that were parallel to that of the standard cortisol preparation (Fig. 2). The slopes of the


Fig. 2. B/Bo (%) of two serial dilutions of the spider monkey urine pool and the cortisol standards to demonstrate

parallelism.

displacement curves for the spider monkey urine pools and the commercial standards were

not different [F (2, 16) = 0.53, NS; F (2, 20) = 2.94, NS]. Recovery of the commercial

standard preparations added to the low concentration pool was 123.6% (r = 1.0; Y = 1.26X +

0.99; P < 0.0001), the medium concentration pool was 104.8% (r = 1.0; Y = 1.08X �3.91;

P < 0.0001) and the high concentration pool was 97.8% (r = 0.993; Y = 0.97X � 4.51; P <0.0001). The assay sensitivity was 3.95 pg.

3.2. Biological validation

A total of 53 urine samples contributed to the analysis of circadian variation in cortisol

levels. Circadian variation was demonstrated for all individuals when samples collected

over 3 days and across an 8-h period were analysed (Fig. 3). The assay was effective in

detecting diurnal variation in cortisol levels [F (4,16) = 4.59, P < 0.001]. Trend analyses

revealed a significant decreasing linear trend across the five time periods [F (1,4) = 9.75, P

< 0.035].

3.3. Visitor numbers

The data presented here were derived from 218 urine samples (which resulted

in 77 data points) collected across 77 days of urine collection. On average we collected

35 urine samples from each monkey (range of 13–51 samples per monkey). We identified

a positive correlation between urinary cortisol and number of visitors (rs = 0.43,

P < 0.001, Fig. 4). A repeated measures ANOVA was then used to compare cortisol

levels from the five subjects across four visitor categories. These were zero (no visitors),

low (1–999), medium (1000–6999) and high (>7000). We corrected for sphericity

problems using Huynh–Feldt correction as recommended by Keppel (1993). We

identified a non-significant result [F(3,12) = 2.57, P < 0.156]. However, further

investigation of the data revealed that the cortisol levels in one adult female showed a

conflicting trend with levels of cortisol decreasing with increasing visitor number

categories. When the data from this individual subject was excluded from the ANOVA, a

significant difference in cortisol levels was observed across the four visitor categories

[F(3, 9) = 10.81, P < 0.002].


Fig. 3. Circadian variation in mean urinary cortisol (�S.E.) excretion in the spider monkeys across five 2-h time

blocks. There was a significant decreasing trend (P < 0.05) in cortisol levels.

4. Discussion

An enzyme-immunoassay was successfully developed and validated to quantify urinary

cortisol in spider monkeys. Immunological validation of the assay was achieved by

showing specificity, accuracy, precision and sensitivity. The biological validation was

confirmed with the detection of a typical diurnal pattern of cortisol excretion in the urine,

which is evident in the plasma of primates (Coe and Levine, 1995). Using the cortisol assay

we demonstrated that increasing visitor numbers are generally associated with increasing

levels of cortisol in spider monkeys. This result indicates that visitors can have a significant

impact on HPA physiology in spider monkeys.

By developing a biologically valid assay to quantify our study we have added to the

growing number of research studies that use physiological indices as a tool (Ziegler et al.,

1995, Whitten et al., 1998, Boinski et al., 1999; Crockett et al., 2000; Dettling et al., 2002).

Recently studies using faecal steroid assays have been used to assess the relationship

between puberty and dispersal in wild female muriqui monkeys (Bracyteles arachnoids;

Strier and Ziegler, 2000) and ovarian cycles in black-handed spider monkeys (A. geoffroyi

rufiventris; Campbell et al., 2001) and our findings contribute to these advances in the study

of steroid hormones in Atelene primates. Collectively, this research is relevant to the

captive breeding and management of the New World monkeys as it provides valuable

information regarding general welfare and reproductive competence, as well as promoting

researchers to explore more refined questions, such as the impact of visitors on physiology.

Our second aim was to increase our understanding of zoo visitor impact by

incorporating a physiological measure. Our study supports previous behavioural research

that visitors can have a meaningful impact on primates in zoos (Hediger, 1969; Chamove et

al., 1988; Fa, 1989; Cook and Hosey, 1995; Hosey, 2000). We did find that as absolute

visitor numbers increased, urinary cortisol increased, which suggests that visitors had an

impact on spider monkey physiology. The latter relationship was positive and it was not

likely attributable to a Type I error as alpha equalled 0.00009. However, the slope of the

data points was not steep, suggesting that although increasing visitor numbers at Chester

Zoo was associated with an increase in cortisol, large numbers of visitors are not a highly

stressful experience for these spider monkeys. One intervening variable that potentially


Fig. 4. Levels of urinary cortisol were positively correlated with the number of visitors (P < 0.001).

mediates a more dramatic HPA response to the impact of visitors is the enclosure design.

A captive animal will be more able to cope with a potentially negative stimulus, such as

exposure to zoo visitors, if it is allowed to respond with active avoidance or escape

responses (Carlstead, 1996). Our study animals had the choice to hide from visual contact

with visitors as the enclosure provided a variety of locations where the spider monkeys

could be concealed from view, including tunnels, thick vegetation and grassy mounds

(see Fig. 1a and b). Previous research has demonstrated that animals which control

their environment, experience less stress than animals with no control (Weiss,

1968). Therefore, spider monkeys within smaller enclosures and with reduced hiding

opportunities may experience more dramatic HPA responses to visitors than that observed

in the current study. Further research is underway at Chester Zoo to ascertain whether

spider monkeys adjust their use of space under conditions of low and high visitor

numbers.

The majority of subjects, four out of five, demonstrated the statistically significant trend

of rising cortisol levels with increasing visitor numbers. One subject however showed the

opposite trend. One possible explanation is that visitors did not affect this subject.

Alternatively, the HPA response of this subject to visitors might have been masked by

additional factors since cortisol is modified by factors in addition to stress such as

reproductive status, age and social dynamics (Clarke et al., 1996; Saltzman et al., 1998;

Gust et al., 2000; Abbott et al., 2003). While our study suggests that visitors do have an

impact on cortisol levels in the majority of spider monkeys the data for all monkeys were

probably influenced by some of these potentially confounding variables since they were out

of our control. However, since sample collection for the study spanned 3 years and

excluded periods of obvious social change or disruption in the group, one might expect the

effect of potential confounds to be minimal.

An elevated cortisol level in itself does not necessarily indicate a negative effect on an

animal’s welfare. The ability for an individual to respond to short-term stressors could even

be seen as beneficial, as the stimulation of the HPA axis would incite positive arousal

(Chamove and Moodie, 1990). Long-term exposure to a stressor (chronic stress) however

can have serious implications for an animal’s welfare (Moberg, 2000). There are therefore

inherent difficulties when interpreting physiological changes, and a multidisciplinary

approach including behavioural and various physiological data has been recommended to

assess welfare of captive animals (Mason and Mendl, 1993).

To conclude, we have validated an enzyme-immunoassay to quantify levels of urinary

cortisol in spider monkeys. The biochemical technique was then applied to assess the

relationship between visitor number and a physiological index in a primate species. Levels

of urinary cortisol increased with rising visitor number suggesting that visitors had a

potential negative impact on our subjects.

Acknowledgements

We are indebted to Zoological Gardens Chester and in particular Research Officer

Dr. Stephanie Wehnelt who acted as an advocate of our project, which entailed regular

collection of specimen samples. We are further indebted to the primate keeping staff,


particularly Andy Lenihan, who started his workday early on a regular basis to allow CMS

access to the spider monkeys. Jason Boyer, Claire Lightfoot and Lindsay Skyner also made

similar early morning sacrifices for the benefit of our research. The research protocol was

approved by the North of England Zoological Society who adheres to all laws pertaining to

the care and treatment of captive animals.

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Documents

Evidence that zoo visitors influence HPA activity in spider monkeys (Ateles geoffroyii rufiventris)