Investigation of productivity in a southern Indian Malabari goat herd shows

opportunities for planned animal health management to improve food

security.

Neil D. Sargison, Sophie A. J. Ivil, John Abraham, Shameem P. S. Abubaker, Andy M. Hopker, Stella

Mazeri, Ilona A. Otter, Nigel Otter

N.D. Sargison, S.A.J. Ivil, S. Mazeri, A. Hopker, University of Edinburgh, Royal (Dick) School of

Veterinary Studies, Easter Bush Veterinary Centre, Roslin, Midlothian, UK. EH25 9RG

J. Abraham, Kerala Veterinary and Animal Sciences University, College of Veterinary and Animal

Sciences, Pookot, Wayanad 673576, Kerala, India.

I.A. Otter, Worldwide Veterinary Service, International Training Centre, Gramya Bhavan/RDO-

building complex, Aruvankadu, 643202, Tamil Nadu, India.

S.P.S. Abubaker, Kerala State Veterinary Council, Peroorkada PO, Thiruvananthapuram 695005,

Kerala, India.

N. Otter, India Project for Animals and Nature, Hill View Farm Animal Refuge, Mavanalla, Masinagudi

PO, Nilgiris 643223, Tamil Nadu, India.

E-mail for correspondence: neil.sargison@ed.ac.uk

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Here we report the objective veterinary clinical measurement of productivity in a representative

southern Indian Malabari goat herd. We show failure to meet pragmatic production targets that

are commensurate with the animals’ genetic potential, or adequate to meet the demands of

global food security. We suggest that this situation may have arisen as a consequence of animal

husbandry constraints and protein undernutrition and imply the involvement of nematode

parasitism. Benzimidazole resistance was detected in Haemonchus spp., showing the need for

better understanding of the principles of sustainable helminth parasite control within the

southern Indian context. Our study highlights the need to understand the true costs of goat

production in seasonally resource poor environments, while also considering its impact on the

overall ecosystem in which the animals are placed. We conclude that pragmatic opportunities for

improvements in goat production efficiency lie in the development of problem-focussed planned

animal health and nutrition management.

Introduction

Goat production is widely considered to be a solution to the challenge of achieving global food

security and has a potentially important role in improving the health and wellbeing of the rural poor

living in marginal environments that present seasonally favourable conditions for agriculture (Pollott

and Wilson 2009). Having evolved as selective browsers in semi-arid or humid ecological

environments, goats are generally more efficient than other domesticated ruminants in their

metabolism and tolerance of poor quality and potentially toxic nutrients and conversion into food

products, hence are adaptable to being the main livestock economic resource in developing

countries (Luikart and others 2001). Small ruminants are further suited to enhancing the livelihoods

of the poor, due to their manageable size, relatively low maintenance requirements, low capital

investment cost, short generation interval and ease of marketing of animals and products, hence

suitability as short-term economic reserves (Singh and Ramkumar 2014).

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The global goal of goats in alleviating poverty is frequently not achieved (Dubeuf 2014). Failures of

goat farming must, therefore, be investigated and addressed before it can become a solution to the

challenge of socioeconomically- and environmentally-sustainable global food security.

The overall aim of our study is to describe pragmatic educational and research priorities to address

failures of goat farming as a socioeconomically sustainable activity within an integrated agricultural

system in seasonally resource poor subtropical areas, using an improved southern Indian Malabari

herd as a pertinent example. We have evaluated the productivity of the herd as a first step towards

identifying the potential for increased food production. We have investigated the primary

constraints to sustainably efficient production, and subjectively assessed if these are pertinent to

inform a model for improved production.

Materials and Methods

General and animal husbandry information concerning the study goat herd

The study herd of about 35 goat does of the Malabari breed had been established in 2006 as a

model system with the aim of showing the role of goats in exploiting natural resources for food

production and demonstrating best-practice production in the southern Indian state of Kerala.

Production targets had been set when the Malabari herd was established, based on matching the

potential performance of the breed which had originally been improved by the selection of animals

through crossing heterosis, then based on production traits, with the estimated available nutritional

resources (Table 1). The purchase price of adult does weighing about 30 kg was about INR 6250

(equivalent to about £62.50) and of the adult buck weighing about 35 kg was about INR 7800. The

encouraging economic model upon which the herd was founded depended upon ‘free’ grazing and

market prices of about INR 6000 for entire male and surplus female goats kids of about 25 kg

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liveweight sold for meat at about 6 months’ old and INR 4500 for cull does weighing about 30 kg.

The herd had been closed since its establishment.

The herd is based in the rural Wayanad district in northeast Kerala, on the Deccan plateau at the

southern end of India’s Western Ghats mountain ranges, at about 900 metres above sea level. The

climate in this subtropical region varies between being warm and dry between about November and

May (daily mean temperatures between about 17oC and 26oC, with daytime high temperatures rising

to about 30oC during April and May and between 10 and 200 mm average monthly rainfall, being

driest between November and March) and warm and wet between June and October (daily mean

temperatures about 20oC and about 500 mm average monthly rainfall). Sharp drops in temperatures

accompany heavy monsoon rains. (Weather data had been collected and recorded locally over

several years.) A large part of the region is covered by deciduous rainforest, with variation in the

growth of different plant species throughout the year, and consequently in composition and

availability of herbage.

Two women are responsible for the care of the goats, each spending about 8 hours daily tending the

animals. All of the goats are housed in splendid, permanent, purpose built buildings, in pens

constructed on wooden-slatted floors, raised about 1.5 m above ground-level. The buildings open

onto a central courtyard, providing shelter from sun, heat and rain. Pens are dry swept clean daily,

and manure removed from under the slats daily by sweeping and washing, while the pens and yard

outside the buildings are periodically disinfected using a hypochlorite formulation. The goats are

generally grouped in separate pens as: lactating does and their kids; pregnant does; non-pregnant

does with yearlings; and bucks in individual pens, with an overall stocking density of about one

animal per square metre.

Between around August and March, the weaned and adult female goats are taken for about 3 hours

per day to free-access grazing, where they feed on whatever natural herbage is seasonally available.

The animals are housed for the remainder of the day. Between about March and May, when the

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availability of herbage dwindles due to drought conditions and also during heavy periods of

monsoon rainfall between June and August, the goats are housed all day. Cultivated forage such as

hybrid Napier grass (Pennisetum spp.) or Jack fruit tree (Artocarpus heterophyllus) leaves, depending

on seasonal availability, is cut and carried to the herd, then fed ad-lib to the housed animals.

Throughout the year, the pregnant and lactating does, other goats, and kids are fed a flat rate of

about 400 g, 300 g and 100 g, respectively of concentrates once per day. The concentrates are

purchased as locally-compounded cattle feed. At the times of year when the adult goats are taken

to ‘free’ grazing each morning, kids less than about 6 months’ old are housed in separate pens, and

only introduced to their dams for about 3 hours during the afternoons. Whenever the goats are

housed all day, the kids have greater, but nevertheless intermittent access to their dams.

Does are taken to the buck for mating whenever oestrus is observed, hence kidding occurs all year

round, regardless of season. There are no specific kidding pens, and the does kid in whatever pens

they are grouped at the time. The navels of the kids are dipped in locally-sourced strong iodine

when they are first seen after birth. Suckling is assisted when it is perceived to be necessary. In the

absence of accurate records, the stockkeepers estimate the annual perinatal kid mortality to be

about 10%. Diarrhoea is reported to be consistently obvious in most of the suckling kids between

one and 12 weeks-old and is perceived as being the main cause of mortality.

There is a tendency to focus on visually obvious health concerns, for example Monezia tapeworms

owing to the obvious appearance of segments in the faeces, and known diseases, for example peste

des petits ruminants (PPR) and haemonchosis. Consequently the goats are routinely vaccinated

using a freeze-dried PPR vaccine (Freeze dried PPR vaccine; Institute of Animal Health and Veterinary

Biologicals), and given ad hoc anthelmintic treatments using fenbendazole and praziquantel

combination tablets (Fentas Plus; Intas Pharmaceuticals).

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Study design

A BVM&S student (SI) spent 4 weeks during August 2014 following the study herd and participating

in daily routine, providing an opportunity to validate the relevant detailed management data

described above and a fresh perspective in collating current production data. During the study

period, the herd comprised of 22 adult does, 8 yearling females and one buck.

The health status of the herd and of individual animals was first determined by focussed veterinary

clinical examination (Sargison and Scott 2010). Our next step in the process of planned animal

health management was to identify the constraints to rationally investigate the primary animal

health problems that were identified. In this case we chose the investigation of linked causes of

poor reproductive performance and kid growth rates, integrating a focussed problem history with

clinical examination of the environment and groups of animals, and using selected ancillary tests to

describe constraints of protein under nutrition and helminth parasitology that were implicated. This

included weighing of animals, determining faecal helminth egg counts (FECs) using a modified

McMaster saturated saline floatation method with a sensitivity of 50 eggs per gram (MAFF, 1986)

and the collection and submission to a local medical diagnostic laboratory (Aebeena Clinical

Laboratory, Kalpetta, Kerala) of serum samples from randomly-selected, representative animals for

analysis of protein concentrations.

A faecal egg count reduction test was undertaken (Coles and others 1992, 2006), treating eight

randomly selected pregnant does, one non-pregnant and non-lactating doe, three lactating does and

three yearlings with 5.0 to 7.5 mg/kg fenbedazole (Fentas Plus; Intas Pharmaceuticals). Seven

pregnant does, two non-pregnant and non-lactating does, three lactating does and four yearlings

acted as untreated controls. Pre and post treatment coprocultures were used (MAFF 1986) to

provide third stage nematode larvae (L3) for morphological identification (Van Wyk and Mayhew

2013). Post treatment reductions in arithmetic mean FECs and 95% confidence intervals were

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calculated using a hierarchical modelling of faecal egg counts package in R (Version 3.0.3) (R Core

Team 2014).

Informed consent

The work of the University of Edinburgh student with the goat herd kept on the Kerala Veterinary

and Animal Sciences University, Pookode was undertaken with ethical approval from the R(D)SVS

and approved in writing by the KVASU Directorate of Entrepreneurship. Faecal samples were

collected from selected individual animals per rectum or directly off the ground. Diagnostic serum

samples were collected from 13 animals by jugular venupuncture. All of the procedures were

undertaken under direct veterinary supervision. The sampling procedures were reviewed and

approved as part of the field work permit (Proceedings of the Directorate of Entrepreneurship

reference KVASU/DE/15436/2004).

Results

Collation of production data

The levels of reproductive performance and kid growth are shown in Table 2. These fail to meet the

pragmatic targets shown in Table 1 for each of the selected indices.

Protein nutrition

The serum protein concentrations of four pregnant, four lactating, five yearling and one non-

pregnant and non-lactating goats are shown (Fig 1). Validated reference ranges for serum protein

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concentrations in goats are not available. However, the serum albumin concentrations of each goat

are below the accepted low ‘normal’ values of 29 to 43 g/l, while the serum globulin concentrations

are all within the accepted ‘normal’ range of 27 to 50 g/l (Matthews, 1999).

Helminth parasitology

The mean FECs (±SEM) of 16 pregnant does, three non–pregnant and non-lactating does, six

lactating does and 8 yearling females were 347 (±70), 367 (±60), 217 (±104) and 463 (±219) epg,

respectively. Monezia spp. eggs were only seen in faeces collected from one yearling female.

The overall arithmetic mean reduction in FEC 14 days after fenbendazole treatment was 75.2%

(89.6% - 40.4%, 95% CI). The arithmetic mean reduction in FEC of the untreated control animals was

12.7% (56.2% -73.1%, 95% CI). Pre-treatment L3 coprocultures were 69% Oesophagostomum, 27%

Haemonchus and 4% short tailed L3 (Teladorsagia or Trichostrongylus). Post fenbendazole treatment

L3 coprocultures were 100% Haemonchus. These results confirm the poor efficacy of the

benzimidazole drug, and according to World Association for the Advancement of Veterinary

Parasitology guidelines (Coles and others 1992; Coles and others 2006) show the presence of

benzimidazole resistance in Haemonchus spp..

Discussion

Our aim was to identify practical and pragmatic opportunities to redress failures of goat farming to

meet the needs for food security and socioeconomic development. Our sampling design was

insufficient to validate the broader potential of southern Indian goat production, but our key findings

are nevertheless pertinent. Kerala has about 1.3 million goats of many different breeds and types

kept under a wide range of management systems, hence it is not possible to define a typical

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southern Indian goat herd. Nevertheless, the Malabari goat breed is a pertinent example due to its

development and genetic improvement from crosses between Arabian and southern Indian

indigenous animals as an adaptation to regional conditions and needs (Radhika and others 2015).

The profitability and sustainability of goat production is influenced by the efficiency of conversion of

primary biological resources to food, fibre, or manure. Therefore, the poor reproductive

performance and slow kid growth rates that have been highlighted in our study, provide an example

of inefficient conversion of natural resources into marketable products; hence of economically

unsustainable and environmentally unfriendly production.

It is not practical to attempt to solve every problem at the first attempt; hence it was necessary to

prioritise key areas. Our study has identified a need to determine the balance between the cost of

labour inputs required to tend animals on free-access herbage and its nutritional value, while also

considering the impact of the goats on the overall ecosystem to which they belong. We have shown

needs to evaluate the response to and cost benefits of nutritional management and nematode

parasite control (Sargison and Scott 2010) with reference to sustainability.

Within the context of Indian goat production, we consider that the poor reproductive performance

demonstrated in our study may be a consequence of the goats being in poor body condition and

negative nutritional balance. Extrapolating from the theory of beef cattle reproductive management

(Mossman and Hanly 1977), it can be argued that the consequences of female goats failing to reach

a critical minimum weight as a proportion of their mature weight by the age at which they are first

mated are twofold: some do not conceive; while those that do so become underweight and are thus

in poor body condition at parturition due to the nutritional demands of pregnancy, and subsequently

at the time of rebreeding due to the further requirements for lactation. Most of these animals then

fail to show oestrus behaviour, have low ovulation rates, or cannot maintain pregnancy. Hence it is

not possible to achieve their target 365-day rebreeding interval. Furthermore, the consequent

combination of low numbers of replacement female animals and a high involuntary culling rate,

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demonstrated by our study, impede genetic improvement through the selection of the best

performing individual animals.

The low albumin concentrations in the study goats may be a result of long-term poor rumen

degradable protein (N) nutrition, or endogenous protein loss. In this case, the manner whereby the

serum albumin concentrations of each goat were low, in the absence of raised globulin

concentrations indicative of chronic inflammatory disease, broadly supports the former explanation

(Henshaw 1995), although this could not be formally proven. Nevertheless, our findings suggest that

the poor body condition and growth rates may be primarily due to inadequate nutritional

management, in part as a consequence of seasonal variation in quality and availability of herbage.

One practical approach to enable efficient utilisation of seasonally-available natural resources is to

introduce a compact, seasonal kidding pattern, following the model that is prerequisite for pastoral

cattle production (Holmes 2001). This necessitates home-bred animals first kidding at one or two

years-old. Two year-old first kidding imparts the potential benefit of their being more mature and in

better body condition when they are mated, with a knock on effect on their life-long reproductive

performance and longevity. A compact kidding period enables targeted disease management, for

example helminth control, and more precise grazing and nutritional supplementation management,

in line with the global move towards precision livestock farming systems (Wathes 2010). However,

before promoting such a fundamental change in goat husbandry, it is first necessary to understand

the seasonal nutrient availability and deficiencies in conjunction with compounding effects of

infectious disease threats.

The nutritive values of a range of natural herbage that is freely available in southern India and other

subtropical environments, and of cultivated crops, are well known and the principles of ration

formulation are understood (Devendra 1981). However, our study highlights the general principle

that the nutritive value of the ration that is actually fed or ingested may be misjudged due to

seasonal variation in the availability of nutrients, poor understanding of the energy cost associated

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with walking to and from free grazing, or changes in availability as a consequence of urbanisation

and other demands on grazing and crop producing land. High levels of once-a-day concentrate

feeding to compensate for seasonal variations in availability of free access cultivated herbage, may

cause ruminal acidosis, potentially compounding the problem by reducing the efficiency of digestion

of natural herbage (Ram and others 2007), although this was not formally evaluated. Similar

considerations apply to the growing practice in southern India of feeding goats energy crop by-

products. There is therefore a need for better understanding of the nutritive value of herbage fed to

goats, of the concept of a balanced ration, and of the effects of concentrate feeding on the efficiency

of digestion of primary natural nutrient resources.

Referring to unpublished historical FEC data for the herd (Dr John Abraham, personal

communication), the FECs occurring in August, at a time when H. contortus FECs usually start to

increase, were considered to be indicative of a potentially significant nematode parasite burden,

although it is acknowledged that as in many aspects of planned animal health management, this

interpretation is highly subjective and formally unproven. There has been an historic dependence

on benzimidazole anthelmintics for the control of haemonchosis in southern Indian goat herds, and

there have been reports of benzimidazole resistance (Manikkavasagan and others 2015). The

importance of anthelmintic drug inefficacy identified in our study extends beyond its implications for

roundworm control in goats, because Haemonchus contortus is also a parasite of co-grazed sheep

and cattle in southern India (Chaudhry and others 2015). Anthelmintic resistance is often considered

to occur first in goats, due to their intrinsic immune responses to nematode parasites and

pharmacokinetics of drug absorption and elimination (Hoste and others 2010) imposing a

significantly higher selection pressure.

We have identified a tendency to focus upon visually obvious indices of infectious diseases and

established perceptions of threats to efficient goat production. This approach encourages remedies

such as the ad hoc anthelmintic treatments using praziquantel and fenbendazole combination

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tablets. The irrational perception of a need to administer praziquantel treatments for Monezia

expansa tapeworms biases the choice of anthelmintic drug for the control of H. contortus towards

using a combination product containing a benzimidazole anthelmintic drug, which we have shown to

be ineffective. Furthermore, the use of anthelmintic drugs in a standard dose rate tablet

formulation presents a high risk of exposure of the helminths to sub-therapeutic drug

concentrations, which may further select for anthelmintic resistance (Besier and Hopkins 1988). This

scenario is unhelpful in addressing efficient and sustainable infectious disease control needed to

ensure food security and shows clear needs to develop objective approaches to place health

management of southern Indian goats in context and develop control programmes integrating

responsible medicines use.

Hands-on involvement with the activities of the study herd of Malabari goats enabled the collection

and interpretation of production and animal health management data in a unique and

unprecedented manner. Our results show that productivity of the study herd is both economically

unsustainable (because it permit neither the maintenance of the closed herd, nor iterative genetic

selection within the herd), and environmentally-unfriendly (owing to the imbalance between food

production, degradation of the natural environment and greenhouse gas production). We have

identified basic animal husbandry and animal health problems contributing to failure to meet

pragmatic production targets. Accurate data recording is important in improving global livestock

production efficiency. Our results highlight the need for future work on the themes of nutritional

and reproductive management, and sustainable helminth control as next steps towards addressing

the global need for efficient livestock production.

Acknowledgments

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We are grateful for the support of Zoetis in enabling and encouraging the University of Edinburgh,

Royal (Dick) School of Veterinary Studies’ engagement in India in developing educational resources

for livestock farmers and keepers. The support and assistance of the University of Edinburgh India

Liaison Office, Mumbai, was important in enabling the work to be undertaken. The assistance of

colleagues at the Kerala Veterinary and Animal Sciences University and of the farm staff caring for

the Malabari goat herd is also gratefully appreciated.

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Liveweight at 12 months’ old 28 kgAdult doe liveweight 31 kgMean kid birthweight 1.6 kgKidding interval Once a yearAverage litter size 2.1 kidsAverage age at first kidding 19 to 21 months

TABLE 1: Pragmatic production targets for the Malabari goat herd, that were based on matching the

potential performance of the genetically improved breed with the estimated available nutritional

resources. The information presented in this table is based on an unpublished document titled ‘goat

rearing in Kerala’ that was produced by the KVASU prior to the establishment of the goat herd. The

information presented in this publication is similar to that reported by Verma and others (2009).

Performance index Actual production Pragmatic targetKids reared annually per lactating doe

1.0 kid 2.1 kids

Mean 4-week-old kid weight

About 4.0 kg Between 6 and 7 kg

Mean weight of adult does

27.3 kg (±1.2 kg SEM) 31 kg

Mean weight of yearling goats, with a mean age of 15 months

11.1 kg (±0.7 kg SEM) About 30 kg

Kidding pattern and interval

Kidding occurs over a protracted period of time, being all year round. The actual mean kidding interval could not be determined from the available records.

365 days over a short period of time

16

354

355

356

357

358

359

360

361

362

363

Mean age of the adult does

About 3 years, with involuntary culling mostly due to failure to re-breed.

More than 5 years, giving scope for voluntary culling.

TABLE 2: Production data for the study goat herd and tenable targets for Malabari goats kept in

comparable environments.

FIG 1: Serum protein concentrations of representative pregnant adult does (n=4), lactating adult

does (n=4) and yearling female goats (n=5).

17

364

365

366

367

368

369

370