Ž .

Applied Animal Behaviour Science 63 1999 65–77

Long-term effects of tryptophan on behaviouralresponse and growing-furring performance in silver

ž /

fox

Vulpes

ulpes

Kirsti Rouvinen

)

, Shannon Archbold

, Sandy Laffin

,Mikko Harri

Department of Animal Science, No

a Scotia Agricultural College, P.O. Box 550, Truro, No

a Scotia,Canada B2N 5E3

Department of Applied Zoology and Veterinary Medicine, Uni

ersity of Kuopio, Kuopio, Finland

Accepted 18 November 1998

Abstract

Ž .

The effects of dietary tryptophan TRP supplementation on behavioural response, bodyweight, feed consumption, and winter fur development was assessed on silver fox pups from July

Ž .

28 until December 5. Ten males and ten females received a commercial fox ration control and 10

Ž .

males and 10 females the same ration supplemented with TRP 1.2 g

MJ ME . Dietary TRPsupplementation increased the consumption of protein and gross energy in September andNovember and total DM in September. The male foxes also consumed more feed and gained moreweight than the females throughout the trial. Dietary TRP supplementation did not affect bodyweight gain, initiation of winter fur growth or fur quality in the test groups. There was a trendtoward later priming of fur in the TRP supplemented group. The number of contacts with thenovel object increased and the latency time until contact with the tidbit and the novel objectreduced towards the end of the experiment. In the tidbit test, dietary TRP supplementation reduced

Ž . Ž .

the latency time of the females 40.4 s compared with the non-supplemented females 58.0 s , the

Ž . Ž .

TRP supplemented males 51.7 s , and the non-supplemented males 47.6 s,

0.001 . In the

Ž .

novel object test, the latency time of the TRP females 32.5 s was likewise reduced compared

Ž . Ž .

with the control group females 46.9 s and TRP group males 44.0 s being comparable to the

Ž .

control group males 38.5 s,

0.029 . It appears that dietary TRP supplement reduces fear andenhances exploratory behaviour in the female silver fox. This is likely due to the female beingmore sensitive to the imbalance between TRP and other large neutral amino acids, the supplementleading to increased brain serotonin synthesis. Further research needs to elucidate the effects of

)

Corresponding author. Tel.:

1-902-893-6646; fax:

1-902-895-6734; e-mail: k.rouvinen@nsac.ns.ca0168-1591

$ - see front matter

Ž .

PII: S0168-1591 98 00241-X

( )K. Rou

inen et al.

Applied Animal Beha

iour Science 63 1999 65–77

dietary TRP on the pineal function due to potential interference with seasonal breeding and furringcontrolled by the photoperiod.

Keywords:

Fear; Anxiety; Fox; Tryptophan; Fur farming

1. Introduction

Ž .

In his analysis of welfare of farmed fur animals, Wiepkema 1994 emphasizes thatfear of humans and infanticide are the main welfare problems in farmed foxes. Improvedhuman–animal relationship has thus become the focus of much current research. Themost long lasting studies carried out since 1967 in Novosibirsk, Russia, have concen-

Ž .

trated on the evolutionary aspects of domestication of the silver fox

Vulpes

ulpes

through selection for non-fearful response toward humans Belyaev, 1979; Osadchuk,

1993; Trut, 1995 . In recent years, more emphasis has been placed on the endocrine

Ž .

regulatory mechanisms of the behaviour of the domesticated foxes Popova et al., 1991 .As a result of this intensive selection, the Novosibirsk silver fox population now exhibitsseveral behavioural and morphological characteristics typical of domestic animals, such

Ž .

as having a prolonged primary socialization period Belyaev et al., 1984 , seeking

Ž .

human contact, and having curved tails and piebald colour patterns Trut, 1995 .The domestication process has also produced fundamental changes in the foxes’reproductive physiology and neuroendocrinology. Compared to the non-selected controlgroup, the silver fox vixens selected for tame behaviour ovulate more eggs, conse-quently having a higher number of corpora lutea and higher levels of progesterone

Ž .

through estrus and most of the preimplantation period of pregnancy Osadchuk, 1993 .The tame silver foxes also have more of the neurotransmitter serotonin and its

Ž .

metabolite, 5-hydroxyindole acetic acid 5-HIAA , in their midbrain and hypothalamus

Ž .

Popova et al., 1991 . The activity of the enzyme responsible for serotonin breakdown

Ž . Ž

monoamine oxidase, MAO is also significantly lower in the tame population Popova

et al., 1991 . This strongly indicates the involvement of the brain serotonergic system inincreasing docility and reducing fear in the silver fox.

Ž . Ž .

The central nervous system CNS synthesises serotonin 5-hydroxytryptamine from

Ž .

its dietary precursor tryptophan Rodwell, 1979 . This indispensable amino acid hasbeen demonstrated to have psychopharmacological activity and be effective in manage-ment of aggression and unwanted behaviours in humans and a variety of species of

Ž .

domestic, laboratory and zoo animals see the work of Mench and Shea-Moore, 1995 .In the swine, dietary TRP supplement has been shown to increase 5-hydroxyindoleconcentration in different brain regions, improve feed consumption and growth perfor-

Ž .

mance and reduce stress response Henry et al., 1996 . When excess tryptophan isavailable in the animal’s diet compared to other large neutral amino acids, such astyrosine, phenylalanine, leucine, isoleucine and valine, which compete for entry to thecentral nervous system across the blood–brain barrier, more tryptophan enters the brain

Ž .

Leathwood, 1987 . When tryptophan is over-represented in the CNS, more of it will beconverted to serotonin since the enzyme responsible for this conversion, tryptophan

Ž .

hydroxylase, is not saturated under normal conditions Rogers, 1995 .

( )K. Rou

inen et al.

Applied Animal Beha

iour Science 63 1999 65–77

Serotonin is also an important substrate for the pineal gland in the synthesis of

Ž . Ž .

melatonin

-acetyl-5-methoxytryptamine Dubocovich, 1991 . The most importantfunctions of melatonin in seasonally breeding and furring species are the regulation of

gonadal activity mink: Ellis, 1985; Valtonen et al., 1992; blue fox: Smith et al., 1987;

silver fox: Connor, 1988; ferret: Ryan and Volk, 1995 and the initiation of winter fur

growth mink: Allain and Rougeot, 1980; Rose et al., 1984; silver fox: Connor, 1988;

blue fox: Jarosz and Szeleszczuk, 1995; ferret: Nixon et al., 1995 . It is also known that

Ž .

melatonin can block ACTH and thus inhibits stress response Rodwell, 1979 . ACTH is

the key hormone known to regulate the period of inactivity in hair follicles Ryder,

1973; Rose and Sterner, 1992; Rose, 1995 . It appears therefore that by blocking theeffects of ACTH, melatonin is able to initiate winter fur development. Supplying theCNS with more serotonin may thus increase melatonin synthesis and consequently havean enhancing effect on winter fur development.The first hypothesis of our study was that increasing dietary levels of tryptophan bylong-term supplementation will increase the level of serotonergic neurotransmission inthe brain and consequently affect the foxes’ behaviour by inducing docility and reducingfear. The second hypothesis was that increasing the long-term availability of tryptophanand consequently serotonin in the CNS would lead into increased melatonin synthesis bythe pineal gland and therefore advanced winter fur development. The objective of theproject was to study the long-term effects of dietary tryptophan amino acid supplementa-tion on behavioural response, feed intake, body weight gain, and winter fur developmentin silver fox.

2. Materials and methods

2.1. Animals

The study involved 40 silver fox pups, 20 males and 20 females, born in the spring of

1997. Ten males and ten females were fed a control diet Purina Fox Developer,

Clarence Farm Services, Truro and 10 males and 10 females were fed a tryptophansupplemented test diet. The pups originated from 14 litters with littermates of both sexesrandomly assigned to the two treatment groups. The foxes were housed in individualpens in a single-aisle shed subject to natural daylight conditions. They had ad libitumaccess to water from a nipple drinker and feed from a hopper. General care of animalsand their handling during experimental protocols were according to the guidelines of the

Ž .

Canadian Council on Animal Care 1993 .

2.2. Diet preparation and analysis

The tryptophan diet was prepared from the control diet by adding 10 times the

recommended amount of the tryptophan amino acid

-tryptophan 98.5% pure, Heart-

. Ž

land Lysine, Chicago, IL . The tryptophan requirement for the mink 0.12 g

MJ ME,

Børsting and Clausen, 1996 was used as a guideline since no current recommendationexists for the silver fox. This equalled 16 g of the amino acid per kg pellets, which was