animals

Article A Cow–Calf Farming System Fully Adapted to Elevation and Harsh Conditions in ()

Ramon Armengol 1 , Marta Bassols 1 and Lorenzo Fraile 1,2,*

1 Department of Animal Science, ETSEA, University of Lleida, 25198 Lleida, ; [email protected] (R.A.); [email protected] (M.B.) 2 Agrotecnio Research Center, ETSEA, University of Lleida, 25198 Lleida, Spain * Correspondence: [email protected]; Tel.: +34-973-702-814

Simple Summary: Optimizing the use of natural resources in cattle production is a concern of the beef meat industry and consumers. Areas with scarce resources or adverse environmental conditions can efficiently take advantage of extensive systems with local breeds. These local breeds are adapted to the environment and can give optimal productive yields. The aim of this work is to explain the project of the Bruna d’Andorra, a local breed under an extensive cow–calf system in Andorra, as an example of local farming and marketing of its meat products. Andorra is a sovereign landlocked microstate in the eastern (Europe) that consists predominantly of rugged mountains and harsh weather conditions for livestock farming. This work describes the evolution of the Bruna d’Andorra population during the period of 2000–2020 focusing on the main meat productive and reproductive performance achievements. Finally, the plans for the future of the project are focused on optimizing a highly sustainable and environmentally friendly farming system.

  Abstract: The use of natural resources is an important topic to optimize the efficiency of cattle production. The purpose of this work is to describe the project of the Bruna d’Andorra; a local cow Citation: Armengol, R.; Bassols, M.; breed under an extensive cow–calf system in Andorra (Europe), as an example of local farming Fraile, L. A Cow–Calf Farming and marketing of its meat products in an area with adverse environmental conditions. This breed System Fully Adapted to Elevation and Harsh Conditions in Andorra is located in Andorra, a microstate that consists predominantly of rugged mountains and harsh (Europe). Animals 2021, 11, 611. weather conditions. The cow–calf Bruna d’Andorra extensive system is thoroughly described and https://doi.org/10.3390/ani11030611 productive and reproductive performance, compiled over 21 years (2000–2020), has been analyzed by years with the Chi-square test or ANOVA to compare proportions or means, respectively, and Academic Editors: Antonino Di regression analysis was used to decipher evolution across years. The results show a population Grigoli and Adriana Bonanno with a census large and stable enough to avoid inbreeding. Moreover, a sustained improvement of the productive performance and maternal fitness has been observed along the studied period for Received: 15 January 2021 Bruna d’Andorra. The work concludes that local breeds can achieve sustainable animal production, Accepted: 23 February 2021 especially when farmers, public administration and commercial circuits in the area agree to cooperate Published: 26 February 2021 on such projects. The study also concludes that the Bruna d’Andorra cow breed can still improve in meat and reproductive performance. Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in Keywords: ruminants; beef cattle; extensive production; local breed; Bruna d’Andorra published maps and institutional affil- iations.

1. Introduction Mountain farming livestock has attracted a wide research worldwide in the past 30 Copyright: © 2021 by the authors. Licensee MDPI, Basel, . years. These pasture-based and small-scale livestock farming systems can be considered This article is an open access article as the main source of livelihood in the mountain primary sector, ensuring socioeconomic distributed under the terms and sustainability and biodiversity in rural communities [1,2]. For the last 25 years, scientific conditions of the Creative Commons research has been carried out in areas close to Andorra with cattle breeds adapted to high Attribution (CC BY) license (https:// mountain pastures, such as Bruna dels Pirineus (BP), Parda Alpina (PA), Gasconne (G), creativecommons.org/licenses/by/ Aubrac (A), Limousin (L) or Salers (S) in order to improve their genetics, productivity or 4.0/). meat quality [3–7].

Animals 2021, 11, 611. https://doi.org/10.3390/ani11030611 https://www.mdpi.com/journal/animals Animals 2021, 11, x 2 of 19

Aubrac (A), Limousin (L) or Salers (S) in order to improve their genetics, productivity or meat quality [3–7]. Andorra, officially Principat d’Andorra (Principality of Andorra), is a sovereign land- locked microstate on the Iberian Peninsula in the eastern Pyrenees that is bordered by to the north and Spain to the south (Figure 1). It has an area of 468 km2 and a

Animals 2021, 11, 611 population of approximately 77,000. Andorra la2 of Vella 18 , its capital, has the highest elevation of any European capital at 1023 m. Andorra’s territory is divided in seven parishes, con- sistsAndorra, predominantly officially Principat d’Andorra of rugged (Principality mountains, of Andorra), is aand sovereign the average elevation is 1996 m. Andorra landlocked microstate on the Iberian Peninsula in the eastern Pyrenees that is bordered byhas France alpine to the north, continental and Spain to the south, and (Figure oceanic1). It has an areaclimates of 468 km.2 andThe a climate depends on elevation. The cli- population of approximately 77,000. Andorra la Vella, its capital, has the highest elevation ofmate any European is characterized capital at 1023 m. Andorra’s by territory convective is divided in sevenand parishes, abundant consists rains during the spring and summer, predominantly of rugged mountains, and the average elevation is 1996 m. Andorra has alpine,which continental, can andlast oceanic until climates. autumn. The climate Winter, depends on elevation. however, The climate is ischaracterized by a great amount of snow- characterizedfall. The by temperature convective and abundant regime rains during is the broadly spring and summer, characterized which can by a temperate summer and a long last until autumn. Winter, however, is characterized by a great amount of snowfall. The temperatureand cold regime winter, is broadly characterizedwhich is by in a temperate keeping summer with and a long the and mountainous cold terrain of the country [8]. winter, which is in keeping with the mountainous terrain of the country [8].

Figure 1. Location of Andorra (green circle) in Europe (dark grey). Source: https://en.wikipedia. org/wiki/File:Location_Andorra_Europe.pngFigure 1. Location of Andorra. (Accessed (green on 29 September circle) 2020). in Europe (dark grey). Source: https://en.wikipe-

dia.org/wiki/File:Location_Andorra_Europe.pngTraditionally, Andorra based its economy on pasture and small-scale livestock. farming(Accessed on 29 September 2020). systems that mainly included sheep, horses and cattle. However, since the 1950s, the pri- mary sector has been losing importance. Nowadays, the tertiary sector currently represents 80% of AndorranTraditionally, Gross Domestic Andorra Product (GDP), based with tourism its being economy the mainstay on of pasture and small-scale livestock farm- the economy. Eight to nine million people visit it every year, attracted by its status as a taxing heaven, systems its ski resorts, that and themainly trade price included differential with sheep, neighboring horses countries [ 9and]. cattle. However, since the 1950s, the Only five percent of the land is arable, and tobacco is the main crop. Farming is based on anprimary extensive and sector semi-extensive has pasture been system losing with a clearimportance. and ancestral purpose: Nowadays, the the tertiary sector currently rep- subsistence of its population in one of the most mountainous and remote areas of Europe (threeresents aptitudes: 80% work, of meat Andorran and milk). With Gross the entry into Domestic the modern era Product of the animal (GDP), with tourism being the mainstay productionof the systemeconomy. (~1950s), bovine Eight livestock to becamenine a singlemilli goal,on which people was the breeding visit it every year, attracted by its status as a of calves, with an extensive and semi-extensive cow–calf farming system. These calves weretax weaned heaven, at 5–6 months its ski of age resorts, and sold to and Spanish the producers, trade where price they finished differential with neighboring countries [9]. Only five percent of the land is arable, and tobacco is the main crop. Farming is based on an extensive and semi-extensive pasture system with a clear and ancestral purpose: the subsistence of its population in one of the most mountainous and remote areas of Europe (three aptitudes: work, meat and milk). With the entry into the modern era of the animal production system (~1950s), bovine livestock became a single goal, which was the breed- ing of calves, with an extensive and semi-extensive cow–calf farming system. These calves were weaned at 5–6 months of age and sold to Spanish producers, where they finished their conventional fattening phase. The calves were slaughtered in Spain and the meat was fully marketed in conventional Spanish circuits. Until year 2000, the breeds that made up the bovine population of Andorra were purebreds and crosses of BP, L, G, A and Charolais. Breed selection, crossbreeding, and bovine candidates to become cows and bulls only depended on the farmers’ subjective criteria, and it was never based on technical data. Thus, the diversity in the final product varied widely and the production parameters were not controlled. In 1999, the national association (Associació de Pagesos i Ramaders d’Andorra) (APRA) [10] and the Government of Andorra (GA) joined forces to create Ramaders d’An- dorra, S.A. (RASA) with a common long-term project named Carn de Qualitat Controlada Animals 2021, 11, 611 3 of 18

their conventional fattening phase. The calves were slaughtered in Spain and the meat was fully marketed in conventional Spanish circuits. Until year 2000, the breeds that made up the bovine population of Andorra were purebreds and crosses of BP, L, G, A and Charolais. Breed selection, crossbreeding, and bovine candidates to become cows and bulls only depended on the farmers’ subjective criteria, and it was never based on technical data. Thus, the diversity in the final product varied widely and the production parameters were not controlled. In 1999, the national association (Associació de Pagesos i Ramaders d’Andorra) (APRA) [10] and the Government of Andorra (GA) joined forces to create Ramaders d’Andorra, S.A. (RASA) with a common long-term project named Carn de Qualitat Con- trolada d’Andorra (Quality Control Meat of Andorra) (CQCA) and registered the label. In 2000, the GA approved a new law of agriculture and livestock and promoted the cre- ation of the Escorxador Nacional d’Andorra (National Slaughterhouse of Andorra) (ENA) following the European Union (EU) regulations. In 2006, after an initial work of breed selection and technical criteria, an official rule issued by the GA created the Genealogical Card for Bruna d’Andorra Bovine Breed (BA), set the technical criteria for genetics of this breed and the staff responsible for this program [11]. In 2009, the GA applied for the “IGP Carn d’Andorra” label in the EU, describing that the meat products included in the label must be from pure BA breed or BA cow crossed with other beef breeds. The label “IGP Carn d’Andorra” was finally accepted and registered in 2009. The BA breed is genetically very closely related to the BP, an autochthonous beef breed located in the mountainous areas of Catalonia (Northeastern Spain) and PA, an autochthonous beef breed located in the mountainous areas of Aragon (Northeastern Spain). The BP and PA breeds originated from the cross of native cattle with imported old-type Brown Swiss individuals during the first decades of the 20th century. After that, animals were empirically selected for meat production purposes. BP and PA are typically reared under extensive conditions for the production of beef calves with an average carcass weight at slaughter of 330 kg at ~12.5 months of age [5,12]. The CQCA project and IGP Carn d’Andorra are based on the following pillars: unifi- cation of the BA breed, genetic improvement, health improvement, maximum use of the country’s natural resources, and full internal marketing of the meat. The main goal of this strategic project of national interest is to achieve a homogeneous bovine population of a typical local breed from Andorra, well adapted to the mountain pastures of the country, and able to maximize the use of natural resources in a sustainable way. This system of cattle production includes the breeding and fattening of calves, obtaining replacement animals, the slaughter of animals, and the marketing of their high-quality meat in the Andorran territory. The project includes BA cows and bulls, L bulls as breeders, and BA or crossed Bruna d’Andorra × Limousin (BA × L) males and females for fattening. The aim of this work is to reflect the evolution of BA population, meat productive performance, and main reproductive data that have been achieved during this 21-year period (2000–2020). A second objective is to explain the plans for the future of the CQCA project as a highly sustainable and environmentally friendly farming system.

2. Material and Methods Ethical Statement All the data used in this study came from historical data using standard production procedures.

2.1. Cow–Calf System in Andorra The traditional farming system in Andorra is extensive and semi-extensive cow–calf grazing, under mating as the only reproduction strategy, and a long pre weaning period (~4–6 months). After a cold and snowy winter (the end of November to the beginning of March) where all bovines are housed indoors down in the villages, all the bovines are set free to the fields nearby the farms and calving season begins (March–June). Animals can be moved indoors nightly depending on the weather conditions, and cows close to Animals 2021, 11, 611 4 of 18

Animals 2021, 11, x parturition are kept in the farm. After June, all animals from all farms that belong to the 4 of 19 same parish are grouped, forming a big herd of approximately 200 to 400 mature cows, calves, and bulls each. This big herd will be grazing and pasturing the high mountains of Andorra under the supervision of a vaquer (cowboy in Catalan) and in cooperation with thewith farmers the (owners).goal to achieve The vaquer a isuniform responsible distribution for controlling of the calvings animals throughout but also for the year. However, deciding where to graze the herds, which depends on the weather and the vegetative stateseasonality of the pastures. is always Therefore, present,the vaquer andis two a key calvin figure ing maximizingseasons are the common: resources of spring and autumn. In highSeptember–October, mountain pastures. During animals this period, are sorted mating according is possible. Adultto the cows farm and they bulls belong are to and transferred alwaysto the together, fields withclose the to goal the to farm achieve for a uniformgrazing distribution until the of strong calvings cold throughout weather comes again. This the year. However, seasonality is always present, and two calving seasons are common: springsystem and includes autumn. In two September–October, important movements: animals are sorted the accordingbeginning to the an farmd end they of the high mountains belonggrazing to and season. transferred This to movement the fields close is carried to the farm out for by grazing moving until the the stronganimals cold through walk-through weatherroads comesand trails, again. except This system for some includes farms two important that have movements: to move the the beginning animals through the big city andto get end to of thethe high high mountains mountains grazing area season. or back This to movement the farm. is carried In these out situations, by moving part of the transport the animals through walk-through roads and trails, except for some farms that have to moveis by the truck. animals During through these the big movements, city to get to young the high bu mountainsll selection area ortakes back place, to the and the ones selected farm.are sent In these to situations, the genetic part ofcenter. the transport Animals is by truck.are se Duringlected these to movements,enter the youngfattening units and are de- bullwormed, selection vaccinated, takes place, and have the ones a blood selected sample are sent taken, to the genetic and heifers center. Animals are evaluated are for replacement selected to enter the fattening units and are dewormed, vaccinated, have a blood sample taken,(Figures and heifers 2–5). are evaluated for replacement (Figures2–5).

• Calving. • Grazing in the farm fields. • Mating with Bruna d’Andorra bulls at 90-120 days post calving. Spring • Blood sampling for infectious diseases. (March-May) • Vaccination/Deworming.

• Grazing High Mountains. Summer • Grouping in a big-collective herd. • Mating with Bruna d’Andorra bulls at 90-120 days post calving. (June- September)

• Calving. • Grazing in the farm fields. Autumn • Mating with Bruna d’Andorra bulls at 90-120 days post calving. • Blood sampling for infectious diseases. (September- • Vaccination/Deworming. November)

• Indoors housing. Winter • Mating with Bruna d’Andorra bulls at 90-120 days post calving. • Hay/Silage+Concentrate, straw and water ad libitum. (November- March)

FigureFigure 2. Management, 2. Management, nutritional, nutritional, and husbandry and protocols husbandry used with prot adultocols cows used (>1 calving). with adult cows (>1 calving). Animals 2021, 11, x 5 of 19

AnimalsAnimals 20202121, 11, 11, x, 611 5 of 18 5 of 19

• Group/Individual. • Indoors or outdoors in the field. Birth • Group/Individual. • Indoors or outdoors in the field. Birth

• Cow-calf system. • Grazing High Mountains from May to October/ Fields from Birth to 120d • October-DecemberCow-calf system. and April to May/Indoors: December-April. of life • NaturalGrazing weaning.High Mountains from May to October/ Fields from October-December and April to May/Indoors: December-April. Birth to 120d of life • Natural weaning. • Entrance to fattening unit. • Deworming and vaccination. • Indoors.Entrance to fattening unit. 120 to 244 d • SeparatedDeworming by and gender. vaccination. of life • Concentrate,Indoors. straw and water ad libitum. 120 to 244 d • Separated by gender. of life • Concentrate, straw and water ad libitum.

• Slaughter. ≥244 d of life • Slaughter. ≥244 d of life

Figure 3. Management, nutritional, and husbandry protocols used during the calf-rearing process of Bruna d’Andorra Bovine Breed (BA) and Bruna d’Andorra × Limousin (BA × L) males and fe- Figure 3. Management, nutritional, and husbandry protocols used during the calf-rearing process of malesFigure destined 3. Management, for fattening. nutritional, and husbandry protocols used during the calf-rearing process Brunaof Bruna d’Andorra d’Andorra Bovine Bovine Breed Breed (BA) and (BA Bruna) and d’Andorra Bruna d’Andorra× Limousin × Limousin (BA × L) males(BA × and L) males females and fe- destinedmales destined for fattening. for fattening.

• Group/Individual. • Indoors or outdoors in the field. Birth • Group/Individual. • Indoors or outdoors in the field. Birth • Cow-calf system. • Grazing High Mountains from May to October/ Fields from October- Birth to 4 mo • DecemberCow-calf system. and April to May/Indoors: December-April. of life • NaturalGrazing weaning.High Mountains from May to October/ Fields from October- December and April to May/Indoors: December-April. Birth to 4 mo of life • Natural weaning. • Grazing High Mountains from May to October/ Fields from October- December and April to May/Indoors: December-April. • MorphologicalGrazing High Mountains and breed fromstandard May e valuationto October/ at Fieldsthe ages from of 6,October 18-24,- >24 months and after 1st calving. 4 to 24 mo of December and April to May/Indoors: December-April. life • DewormingMorphological and and vaccina breedtion standard every evaluation6 months. at the ages of 6, 18-24, >24 • Heifermonths group and after without 1st calving. bull. 4 to 24 mo of life • Deworming and vaccination every 6 months. • Heifer group without bull. • Heifers group With bull. • Morphological and breed standard evaluation>24 mo. and after 1st calving • MHeifersating withgroup Limou With sinbull./ Bruna d’Andorra bulls certified for easy calving. ≥24 mo of life • DewormiMorphologicalng and and vaccin breedation standard every evaluation>246 months. mo. and after 1st calving • Mating with Limousin/ Bruna d’Andorra bulls certified for easy calving. ≥24 mo of life • Deworming and vaccination every 6 months.

Figure 4. Management, nutritional, and husbandry protocols used during the calf and heifer rearing process of BA females destined for cow replacement. Figure 4. Management, nutritional, and husbandry protocols used during the calf and heifer rear- ing process of BA females destined for cow replacement. Figure 4. Management, nutritional, and husbandry protocols used during the calf and heifer rear- ing process of BA females destined for cow replacement. Animals 2021, 11, 611 6 of 18 Animals 2021, 11, x 6 of 19

• Group/Individual. • Indoors or outdoors Birth in the field.

• Cow-calf system. • Grazing High Mountains from May to October/ Fields from October-December Birth to 4 and April to May/Indoors: December-April. mo of life • Natural weaning.

•1st Physical evaluation and Blood testing for infectious disease. • Tansport to genetic selection center (France). 4 to 8-10 • Deworming and vaccination every 6 months. mo of life • Grazing+Concentrate, straw and water ad libitum.

• Stay in the genetic selection center (France) for 5-8 months. • Accurate analysis of the genetic criteria: Blood sampling (for mh gene elimination), anatomical evaluation (incl. reproductive tract and sperm viability) 8-10 to 13- and measurements, productive and meat quality data and breed standards. 16 mo of • Deworming and vaccination every 6 months. life • Grazing+Concentrate, straw and water ad libitum.

• Transport back to Andorra. • Retested at the ages of 18-24 and 36 months. • Entering in a Herd as Bull. ≥13-16 mo • Deworming and vaccination every 6 months. of life • Grazing.

Figure 5. Management, nutritional, and husbandry protoc protocolsols used used during during the the calf calf and and bull bull rearing rearing process of BA males destined for bull replacement.

Autumn and spring pastures in the low attitudeattitude fieldsfields close to the farms were based on planted planted MedicagoMedicago sativa, sativa, Dactylus Dactylus glomerata, glomerata, Festuca Festuca arundinacea, arundinacea, Lolium Lolium perenne, perenne, and andTri- Trifoliumfolium ladino. ladino. SomeSome fields fields were were harvested harvested as as hay hay and/ and/oror silage silage as as feeding feeding source during indoor winter winter season. season. High High mounta mountainsins pastures pastures were were composed composed on on FestucaFestuca airoide, airoide, Hier- Hi- aciumeracium breviscapum, breviscapum, Carex Carex curvula, curvula, Oreochloa Oreochloa disticha, disticha, andand LeontodonLeontodon pyrenaicus pyrenaicus in elevations between 2300 and 2800 m; Festuca eskia, Festuca gautieria, Festuca nigrescens, Festuca ovina, Anthoxanthum odoratum, Achillea millefolium, Trifolium Trifolium alpinum, Trifolium repens, Trifolium pratense, Koeleria Koeleria vallesiana, vallesiana, Thymus Thymus serpyllum, serpyllum, Caluna Caluna Vulgaris, Vulgaris, Lotus Lotus corniculatus, corniculatus, Meum Meum ath- amanticum,athamanticum, Vicia Vicia Pyrenaica, Pyrenaica, Scutellaria Scutellaria alpina, alpina, Festuca Festuca paniculata, paniculata, Asphodelus Asphodelus albus, albus,Iris latifo- Iris lia,latifolia, Paradisea Paradisea liliastrum, liliastrum, Dactylis Dactylis glomerata, glomerata, Avenula Avenula versicolor, versicolor, Campanul Campanulaa scheuchzeri, scheuchzeri, Nardus stricta,Nardus Gentiana stricta, Gentiana acaulis, acaulis,and Trifoliumand Trifolium alpinumin alpinumin were atwere elevations at elevations between between 1600 and 1600 2700 and m.2700 At m. elevations At elevations between between 1400 1400and 2200 and 2200m, some m, some natural natural grazing grazing areas areas were were forested forested and composedand composed of Pinus of Pinus uncinata uncinata andand AbiesAbies alba alba. The. The proportion proportion of of each each plant present present in in thethe pastures alsoalso varied varied on on the the soil soil composition, composition, water water sources, sources, direct direct sunlight, sunlight, and each and year’s each year’sclimatology. climatology. Production Production in dry matter in dry (DM) matter in natural(DM) in pastures natural inpastures Andorra in wasAndorra estimated was estiin 1000mated to 3000in 1000 kg/ha/year to 3000 kg/ha/year [13,14]. [13,14]. Females and males destined for fattening were required to spend at least the firstfirst four months of life with their mother and could not be sent to slaughter before eight months months of life with their mother and could not be sent to slaughter before eight months of of age [11]. They were kept in semi-open fattening units with at least 3 m2/animal and age [11]. They were kept in semi-open fattening units with at least 3 m2/animal and accord- according to their body weight (BW), feeding was ad libitum based on natural concentrate ing to their body weight (BW), feeding was ad libitum based on natural concentrate (cereals, (cereals, legume and oilseeds, minerals, and vitamins), with hay of the mountain grass as a legume and oilseeds, minerals, and vitamins), with hay of the mountain grass as a fiber fiber source, and water (Figure3). Heifers destined for future replacement followed the source, and water (Figure 3). Heifers destined for future replacement followed the same same grazing system and movements as the adults, but in an independent group without grazing system and movements as the adults, but in an independent group without bulls bulls in order to avoid mating too young and the subsequent dystocia and mortality in order to avoid mating too young and the subsequent dystocia and mortality problems problems (Figure4). (Figure 4). Animals 2021, 11, x 7 of 19

It is of highest interest for the GA and RASA to maintain this system as a main char-

Animals 2021, 11, 611 acteristic of the BA breeding system, because it is the most sustainable and 7environmen- of 18 tally friendly for the country.

2.2. Co-Working Government Farmers It is of highest interest for the GA and RASA to maintain this system as a main charac- teristicThe of theproject BA breeding began in system, 2000 with because the aim it is theof producing most sustainable a high-quality and environmentally meat that is stand- friendlyardized forand the officially country. recognized. Since then, the GA and RASA cooperated to obtain an EU high quality meat label. Carn d’Andorra® is a trademark of RASA that is marketed 2.2.under Co-Working the control Government and guarantee Farmers seals CQCA and under the protected geographical indi- cationThe seal project “IGP began Carn in d’Andorra” 2000 with the [15]. aim of producing a high-quality meat that is stan- dardized and officially recognized. Since then, the GA and RASA cooperated to obtain an ® EU2.3. highThe qualityBreed meat label. Carn d’Andorra is a trademark of RASA that is marketed un- der the control and guarantee seals CQCA and under the protected geographical indication seal “IGPThe Carnchoice d’Andorra” of the breed [15 ].that was included in the CQCA project was the BP [16]. How- ever, it was decided not to strictly follow the breed standards established by the BP Asso- 2.3.ciation The Breed(Catalonia) and to create the BA breed. This decision was for two reasons: to fully adaptThe the choice breed of as the much breed as that possible was included to the Andorran in the CQCA productive project wassystem the (adaptability BP [16]. to However,the high mountain it was decided environment not to strictly and follow harsh theweat breedher standardsconditions) established and to create by the a BPbreed with Associationan Andorran (Catalonia) identity andname. to createThis election the BA breed. was agreed This decision by the wasGA forand two RASA, reasons: and to officially fullyadopted adapt in the 2006 breed [11]. as muchBriefly, as possiblethe BA tois thea cow Andorran very adapted productive at systempasturing (adaptability the high moun- to the high mountain environment and harsh weather conditions) and to create a breed tains (strong hooves and claws), obtaining food (wide nose and deep thorax) and feeding with an Andorran identity name. This election was agreed by the GA and RASA, and officiallythe natural adopted vegetation in 2006 of [11 the]. Briefly, area, theis adapted BA is a cow to veryclimatic adapted difficulties at pasturing and theelevation high (rain, mountainssnow, and (stronglow temperatures), hooves and claws), has a marked obtaining mate foodrnal (wide instinct, nose and and deep calves thorax) with and ease. These feedingcows are the brown, natural with vegetation color oflightening the area, isin adapted the eyes, to climaticnose, inside difficulties elbow, and udder, elevation belly, inner (rain,part of snow, limbs, and and low temperatures),perineum. There has amay marked be a maternal degraded instinct, bar along and calves the entire with ease. dorsal line, Theseespecially cows in are males. brown, Mucous with color membranes lightening in are the pink eyes, to nose, orange, inside and elbow, snouts udder, are belly, black. The innerhooves part are of limbs,evenly and pigmented, perineum. round, There may and be uniform. a degraded The bar average along the height entire dorsalis ~135 cm at line,shoulder especially and the in males. thoracic Mucous perimeter membranes is ~190 are cm. pink The to rusticity orange, and factors snouts are are enhanced: black. crest The hooves are evenly pigmented, round, and uniform. The average height is ~135 cm at (especially in males), chin (may be sinuous, but not exaggerated), and thick limbs. The shoulder and the thoracic perimeter is ~190 cm. The rusticity factors are enhanced: crest (especiallyspine should in males),describe chin a rectilinear (may be sinuous, profile but and not uniform. exaggerated), The head and must thick be limbs. wide The with a flat spineforehead, should strong describe jaw, a and rectilinear well-drawn. profile andThe uniform.ears are big, The headwith mustabundant be wide white with hair a inside flatand forehead, eyes are big strong and jaw, vivid. and Horns well-drawn. are in the The sh earsape are of a big, low with lyre abundant and round white section, hair whitish insideand with and the eyes black are big tip and (Figure vivid. Horns6). The are breed in the st shapeandards of a also low lyreconsider and round of high section, interest the whitishsafety of and humans with the (farmers black tip and (Figure tourists)6). The breedand animal standards welfare. also consider Therefore, of high the interest selection pro- thegram safety discards of humans individuals (farmers aggressive and tourists) to and humans animal or welfare. any factor Therefore, that can the selectiondifficult calving programease (i.e., discards gen of muscular individuals hypertrophy—Mh). aggressive to humans The or any project factor also that permits can difficult mating calving for the first ease (i.e., gen of muscular hypertrophy—Mh). The project also permits mating for the first calving with BA bulls negative to Mh (genetic profile: +/+) or L, in order to reduce dystocia, calving with BA bulls negative to Mh (genetic profile: +/+) or L, in order to reduce dystocia, culling, andand calf calf mortality mortality risks. risks. BAxL BAxL calves calves must must be always be always destined destined for fattening for fattening and and are notnot allowed allowed to to become become breeders. breeders.

Figure 6.6.Adult Adult female female and and male male BA BA cattle. cattle. Source: Source: Natà liaNatàlia Montan Montané.é. Animals 2021, 11, 611 8 of 18

2.4. Genetic Improvement of the Breed The BA genetic improvement program focused its efforts on maximizing the strengths of the breed (adaptability to the environment, acceptable productive yields, and good maternal fitness) and minimizing the weak, unwanted, or risky points (gene of Mh, in- breeding, and aggressiveness). The first step and most important point of the program was the selection of the bulls. At the age of eight to 10 months, male calves that were destined to be future bulls were selected as candidates in Andorra and transported to the Genetic Selection UPRA Gasconne Center (Villeneuve de Paréage, France). Trained technicians and veterinarians of the GA carried out this first selection. These males spent five to six months in the center for an accurate analysis of the genetic criteria. The genetic selection included blood sampling (for Mh gene elimination), anatomical evaluation (absence of defects, in- cluding genital tract and sperm viability–quality and quantity) and measurements (height at hock, body length—back, loin and rump—width at shoulders, width and depth at inside elbows, girth of chest, pelvic length and width, sacral-pubis bones length), productive (average daily gain—ADG) and carcass quality data (muscle and bones development), and breed standards. Based on all these measurements, bulls received a final qualification over 100 points. At the age of 14–16 months, these males returned to Andorra as BA bulls certified as breeders if they had successfully passed the test with ≥61 points (Figure5). The genetic data compiled from the bull itself recommended/allowed the bull to remain in the herd where it was born or to be sold/transferred to another herd in order to avoid inbreeding. Bulls were retested at the ages of 18–24 and 36 months. Female calves, destined as future BA cows, never exited Andorra and their genetic selection was based on anatomical (absence of defects), morphological (rump and pin bones for maternal aptitude and meat yield performance parts of best interest) and breed standard evaluation at the ages of 6, 18–24, >24 months, and after their first calving. For safety and management reasons, the evaluation of the females was visual while pasturing and it was carried out by trained technicians and veterinarians of the GA. To be part of the selected BA cows, they were required to obtain 61 points out of 100 in the test. In 2004, the BA breed national contest was created. Every 27 October, the best indi- viduals in the evaluation of the BA breed received a national award in the different age categories. Another annual national event started in 2012: the certified BA bull auction in order to promote the transfer and purchase of the tested and certified BA bulls. These two events are considered to be of national interest and the team responsible for the project takes advantage of those events to explain the breeding and fattening system to the population and promote the meat consumption of BA meat under the label Carn d’Andorra®.

2.5. Health Program Bovines in Andorra are not reared under bio/eco veterinarian and farming rules. However, it is of high interest to all the professionals in the project to feed the animals as naturally as possible, to reduce the use of antibiotics, and to control and eradicate diseases. Bovines from Andorra are free of Brucellosis and have low prevalence (<10%) of Infectious Bovine Rhinotracheitis (IBR), Tuberculosis, Besnoitia besnoiti (GA Veterinarian Service internal data), and Neospora caninum [17]. Bovines older than 180 days received parenteral deworming every six months. Official Veterinary Services consider the risk of parasitism to be high along all the seasons, as cattle share pastures with other domestic (sheep, goats and horses) and wild species (Roe deer (Capreolus capreolus), wild boars (Sus scrofa), chamois (Rupicapra rupicara) and mouflons (Ovis orientalis musimon). Anthelmintic drugs used (Moxidectin 0.2 mg/kg BW SC CYDECTIN® Zoetis Spain, S.L. Alcobendas Spain; Ivermectin 0.2 mg/kg BW SC NOROMECTIN®, Norbrook Laboratories, Ireland or Doramectin 0.2 mg/kg BW SC DECTOMAX®. Zoetis Spain, S.L. Alcobendas Spain) are rotated taking into account the regular (yearly) parasite diagnosis in order to minimize the development of resistance under veterinary supervision. Pregnant cows are vaccinated against Escherichia coli, rota-, and coronavirus in order to prevent neonatal calf diarrhea (Rotavec®, Merck Sharp and Dohme Animal Health, S.L., Animals 2021, 11, 611 9 of 18

Burgwedel, ). Animals destined to the fattening units are parenterally dewormed and vaccinated against Clostridium spp. (Covexin 10®, Zoetis Spain, S.L. Alcobendas Spain) at entry in the unit. Calving ease is reported by the farmer to the official database managed by the GA. Calving ease is scored CE0 to CE4 (CE0, easy; CE1, slight assistance; CE2, moderate assistance; CE3, difficult calving; CE4, extreme difficulty calving, cesarean, or fetotomy). Scores CE3 and CE4 are considered dystocia.

2.6. Slaughter and Meat Products Since the beginning of the project, both the GA and RASA knew that to optimize the sustainability of the final product, the meat had to be processed, sold, and consumed as close as possible from the grazing areas. Thus, the processing and consumption had to be, ideally, within the Andorran territory. That is why the ENA was built in 2000 and the Andorran butchers and restaurants were asked to cooperate, taking part in the project and promoting the consumption of “IGP Carn d’Andorra” meat by the Andorrans and the large number of tourists that visit the country every year.

2.7. Data Compilation and Statistical Analysis The data used for this descriptive study were from official sources of the GA, the RASA, and the ENA. During the study period, these three institutions manage databases with more than 20,000 data points from 47 farms. Data under study are: census (females > 12 months old, bulls, and animals in the fattening units), fattening performance (body weight—BW—at birth (kg), BW at slaughter (kg), average daily gain (ADG) (g/days of life, % meat yield (Kg carcass/kg BW ×100-)), carcass quality based on muscular profile with 6 rates: S (superior), E (excellent), U (very good), R (good), O (fair), P (poor) (SEUROP rating) [18], and reproductive performance (age at first calving, average number of calving, calving ease, interval calving–calving). Data compiled are from pure BA and BAxL breeds. All statistical analyses were carried out using SAS V.9.1.3 (SAS institute Inc, Cary, NC, USA). For all analyses, the individual animal was used as the study unit. The significance level (p) was set at 0.05. The variables included in the statistical analyses were classified as nominal (carcass quality (SEUROP rating), gender, and breed (BA and BAxL breeds)), ordinal (calving ease and year) or continuous: body weight—BW—at birth (kg), BW at slaughter (kg), % meat yield (Kg carcass/kg BW ×100), age at first calving (months), average number of calvings, and interval calving–calving (months). Shapiro Wilk´s and Levene tests were used to evaluate the normality of the distribution of the continuous variables and the homogeneity of variances, respectively. Contingency tables (Chi-square or Fisher exact tests) were used when the association between nominal and ordinal variables was assessed. To study the association between nominal or ordinal variables with the continuous non-normally distributed variables, the Wilcoxon test (with the Mann–Whitney U test to compare each pair of values) was used. To analyze the association between continuous normally distributed variables and nominal or ordinal variables, an ANOVA test (with Student´s t-test to compare each pair of values) was used. Finally, a Pearson or Spearman regression analysis was carried out to decipher the evolution of the year (as a continuous variable) with other normally distributed continuous variables or not, respectively.

3. Results and Discussion The data available cover a total of 21 years (2000–2020). During this period, the yearly population of bovines older than 12 months (cows, bulls, and replacements) ranged between 1008 and 1390 bovines. These data agree with the calculations that the government has for a sustained cow–calf production system considering the feeding yield in high mountain grazing areas. The data analyzed were from 14,128 calvings and 9982 slaughtered males and females, including pure BA and BAxL bovines. The complete data of this study are in the Supplementary Materials for interested readers (Tables S1 and S2). Animals 2021, 11, x 10 of 19

The data available cover a total of 21 years (2000–2020). During this period, the yearly population of bovines older than 12 months (cows, bulls, and replacements) ranged be- tween 1008 and 1390 bovines. These data agree with the calculations that the government has for a sustained cow–calf production system considering the feeding yield in high mountain grazing areas. The data analyzed were from 14,128 calvings and 9982 slaugh- Animals 2021, 11, 611 tered males and females, including pure BA and BAxL bovines. The complete data of10 this of 18 study are in the Supplementary Materials for interested readers (Tables S1 and S2).

3.1. Bruna d’Andorra Population Census 3.1. Bruna d’Andorra Population Census The number and proportion of BA bovines older than 12 months has always in- creasedThe every number year andin a proportionsteady and of controlled BA bovines pace. older In than 2000, 12 Andorra months hashad always a total increased of 384 femalesevery and year nine in a bulls steady selected and controlled for the breed pace.ing In program, 2000, Andorra correspondi had ang total to of39.7% 384 femalesof the bovineand nine population bulls selected of the country. for the breeding In 2020, program,the population corresponding older than to 12 39.7% months of theand bovine con- sideredpopulation for reproductive of the country. aptitude In 2020, consisted the population of 95.4% older of BA than breed 12 months bovines, and 1149 considered females for andreproductive 54 bulls (see aptitude Figure 7 consisted and Table of S1 95.4% for ye ofarly BA detailed breed bovines, data in 1149Supplementary females and Materi- 54 bulls als).(see It is Figure important7 and to Table remark S1 forthat yearly farmers detailed were allowed data in to Supplementary introduce cows Materials).of the BP breed It is becauseimportant it was to remarka genetically that farmers closely wererelated allowed breed toand introduce there was cows a high of the risk BP of breed inbreeding because it was a genetically closely related breed and there was a high risk of inbreeding at the at the beginning of the program. Since 2004, it is forbidden to introduce animals in the beginning of the program. Since 2004, it is forbidden to introduce animals in the genetic genetic program that are not born from a BA cow and bull. Other breeds that complete program that are not born from a BA cow and bull. Other breeds that complete the adult the adult bovine population in Andorra are G, A and L. bovine population in Andorra are G, A and L.

1500

1000

500

0

0 1 2 3 4 5 6 7 8 9 0 1 2 4 5 6 7 8 9 0 0 0 0 0 0 0 0 1 1 1 1 1 2 01 20 20 20020020 20 20020 20 20 20120 20 201320120 20 2012 20 20 Number of females older than 12 months

Figure 7. Evolution of total (blue filled circles) and BA females (red filled squares) older than Figure 7. Evolution of total (blue filled circles) and BA females (red filled squares) older than 12 12 months from 2000 to 2020 in Andorra. months from 2000 to 2020 in Andorra. Between 2005 and 2010, there was an increase in the overall BA bovines that first indicatedBetween the 2005 possibility and 2010, of maintaining there was thean breedincrease census in the and overall avoiding BA inbreeding bovines that problems. first indicatedDuring thesethe possibility years, the of fattening maintaining of BA the increased breed comparedcensus and to avoiding the previous inbreeding years, showing prob- lems.that During the genetic these selection years, the could fattening be carried of BA out increased with the compared best cows andto the bulls. previous It is of years, special showinginterest that to remark the genetic that between selection 2000 could and be 2004, carr anyied out BA with female the entered best cows to the and fattening bulls. It units is ofand special the numberinterest ofto BAremark bulls that not selectedbetween as2000 breeders and 2004, and destinedany BA female to fattening entered was to always the fatteningbetween units zero and and the seven number per yearof BA between bulls not 2000 selected and 2006. as breeders The last and period destined under to studyfat- tening(2011 was to 2020) always shows between a sudden zero increaseand seven in theper BAyear females between and 2000 males and destined 2006. The to last fattening pe- riodper under year (>125 study and (2011 >220, to 2020) respectively) shows a as sudden a consequence increase of in the the increase BA females in BA and calves males born. destinedThis increase to fattening in BA per animals year in(>125 the fatteningand >220, unitsrespectively) relates to as a decreasea consequence in BAxL of the animals, in- creasewith in less BA than calves 100 born. females This and increase males perin BA year animals since 2013 in the and fattening 2015 (for units yearly relates results to seea decreaseTable S1 in in BAxL Supplementary animals, with Materials). less than This 100 change females in theand fattening males per units year breed since composition 2013 and is mainly because of the better calving ease of BA cows and heifers and the elimination of the Mh gene in the BA bulls allows the farmers to decide that the first calving can be the pure BA breed without risk. Another reason is that farmers prioritize the chance to increase the selection of future BA cows than fatten crossed animals with better meat yield. Table S1 in Supplementary Materials shows the yearly decrease of L bulls along the period under study. To sum up, the project began with 18 to 27 L bulls (year 2000 to 2007) and this population is under 10 bulls since 2013. It is important to remark that in years 2019 and 2020, only one L bull was destined for breeding. Animals 2021, 11, 611 11 of 18

3.2. Productive Improvement of the Breed The increase in BA breeder census (heifers, cows, and bulls) guarantees the viability of the genetic program. As a result, some productive parameters such as calving ease (CE0–CE4), average daily gain (g BW/day), meat yield (%), and carcass quality (SEUROP) have all improved over these years. Heifers and young bulls discarded for replacement, removed adult cows and bulls were also introduced in the market as CQCA. The compilation of BW at birth began in 2005. During the whole period studied, males from both breeds under study (BA and BAxL) had a significantly higher BW than females. The average BW was 40.2 ± 4.5 kg for BA males, 42.2 ± 0.8 for BAxL males, 39.2 ± 4.3 kg for BA females, and 40.6 ± 0.8 kg for BAxL females (p < 0.0001). BW has gradually and significantly decreased along all years in both genders and for both BA and the BAxL breeds (p < 0.001) (Figure8A,B). At the beginning of the program (2006–2010), BA female calves averaged ~42 Kg (always over 41 Kg) and since 2016, the BW has always been below 40 kg. In BA male calves, the average BW has decreased irregularly, but decreased from ~43–44 (years 2006–2010) to ~39–40 kg (2016~2020) (For detailed yearly data see Table S2 in Supplementary Materials). In this sense, today’s BA breed calves seem to be lighter than calves from other genetically close related breeds such as BP (44.27 to 46.98 kg BW) [19,20] or PA and Brown Swiss (BS) (~45 Kg BW) [12,21]. Regarding other European breeds, adapted to pasture-based systems, and also common in the Pyrenees mountains, BA calves are lighter than G, with a BW at birth of ~45.3–40.7 Kg [22], but heavier than S or L, with a ~31.8–30.7 and ~28.8–33.5 Kg BW, respectively [23,24]. The authors highlight that the BW reported are from the year 2000 to 2014 for other breeds, so they might have also varied their BW at birth in the last six years. However, we could not find more references. For crossbred BAxL calves, BW has also decreased and has been generally below the pure breed calves. In BAxL female calves, BW decreased from ~41 kg to ~38 since 2016; for BAxL males, the decrease has been from ~42–44 Kg in period 2006–2010 to ~40 kg (see Table S2 for yearly detailed data in Supplementary Materials). On the other hand, it has been known for years that crossbreeding with L can improve calving ease and performance [25]. Thus, the well-known calving ease of the cross breeding with L bulls, the sturdiness, the good productivity, and the good performance, in terms of meat yield and carcass classification, at any age at slaughter [26] caused the decision to include the crossbreeding with L for first parturition BA heifers, but the main goal was to reduce the mortality and dystocia of BA first calving cows. The use of L bulls for crossbreeding in different countries and with dairy breeds has also demonstrated a higher ADG and live weight gain per kg of food consumed than those of any other breed [26]. As expected, males had a significantly higher BW at slaughter than females in both BA (504 ± 61 vs. 420 ± 51 kg) and BAxL (507 ± 59 vs. 425 ± 50 kg) groups (p < 0.001) (Figure9A,B). As an overall result, the age at slaughter is ~365 days for all the animals sent to slaughter. The age and BW at slaughter for females and males of BA and BAxL have shown significant differences between the years under study (p < 0.001), but these differences do not show a consistent trend along the time (see Figure9 and Table S2 for yearly results in Supplementary Materials). Of special interest is the significantly greater age and BW at slaughter of the BA compared to the BAxL between years 2005 to 2007 (Table S2 in Supplementary Materials). These differences are probably due to the fact that it was the first period where the genetic program could discard candidates as future cows and bulls. Thus, after testing and retesting, discarded animals were slaughtered with older ages. The inclusion of these animal data in the slaughtered BA animals has increased the BW at slaughter in this period of time. These between-year differences might be also due to the meat price variation, variability on the feeding cost, and the demand of product depending on market demand. It is important to remark that thousands of tourists visit Andorra, and a priority of the project is to always have CQCA/IGP Carn d’Andorra products to cover the market demand. The total number of visitors to the country is strongly influenced by snow conditions in winter, good weather in summer, and even on which day of the week the holidays are in neighboring countries (France and Spain). All of these factors have an Animals 2021, 11, 611 12 of 18

Animals 2021, 11, x 12 of 19 effect on the demand for meat, especially in hotels and restaurants in Andorra, and are different between years.

A 60

50

40

30

Calf birth weight 20 10 0 7 4 05 08 10 12 15 17 19 0 00 0 0 0 01 0 0 0 2 20062 2 20092 20112 20132 2 20162 20182 2020

B 60

50

40

30

Calf birth weight 20 10 0 7 4 05 08 10 12 15 17 19 0 00 0 0 0 01 0 0 0 2 20062 2 20092 20112 20132 2 20162 20182 2020

Figure 8. Birth weight of calves from BA (A) and BAxL (B) split by males (blue filled circles) and Figure 8. Birth weight of calves from BA (A) and BAxL (B) split by males (blue filled circles) and females (red filled squares) from 2005 to 2020 in Andorra. Calf birth weights decreased linearly across females (red filled squares) from 2005 to 2020 in Andorra. Calf birth weights decreased linearly years for both genders and breed groups (p < 0.0001); and bull calves were consistently heavier than across years for both genders and breed groups (p < 0.0001); and bull calves were consistently heifer calves across breed groups (p < 0.001). heavier than heifer calves across breed groups (p < 0.001). Both genders of the BAxL crossbreed showed a significant improvement along the periodAs regarding expected, the males ADG had and a meat significantly yield (p < higher 0.001) andBW hadat slaughter better performance than females during in both BA (504the fattening± 61 vs. 420 process ± 51 kg) than and BA BAxL animals (507 (p ±< 59 0.001) vs. 425 (Figure ± 50 10 kg)A,B). groups On average, (p < 0.001) BA (Figure males 9A,B). Ashad an an overall ADG ofresult, 1277 the± 175 age and at slaughter females 1031 is ~365± 156 days g/day. for all In the BAxL animals males, sent the ADGto slaughter. Thewas age 1305 and± 175 BW g/day at slaughter and BAxL for femalesfemales averaged and males 1070 of ±BA152 and g/day BAxL (see have Table shown S2 in signifi- Supplementary Materials for yearly detailed results). In contrast, both genders of the BA cant differences between the years under study (p < 0.001), but these differences do not pure breed showed a slight but significant decrease (p < 0.05) of ADG along the period. showThis decrease a consistent in BA ADGtrend might along be the explained time (see because Figure the project9 and priorityTable S2 was for the yearly maternal results in Supplementarycharacteristics and Materials). a better calving Of special ease for interest the pure is breed. the significantly The fact that discarded greater age animals and BW at slaughteras breeders of have the beenBA compared finally slaughtered to the BAxL at older between ages might years also 2005 penalize to 2007 the (Table BA ADG. S2 in Sup- plementaryThe ADG in Materials). pure BA are These lower differences than those reported are prob inably similar due breeds to the such fact asthat BP, it where was the first period74 BP bulls where had the an ADGgenetic of 1630 program g/day [could5] or PA, discar officiallyd candidates reporting 1750as future g/day cows in males and bulls. Thus, after testing and retesting, discarded animals were slaughtered with older ages. The inclusion of these animal data in the slaughtered BA animals has increased the BW at slaughter in this period of time. These between-year differences might be also due to the meat price variation, variability on the feeding cost, and the demand of product depend- ing on market demand. It is important to remark that thousands of tourists visit Andorra, and a priority of the project is to always have CQCA/IGP Carn d’Andorra products to cover the market demand. The total number of visitors to the country is strongly influ- enced by snow conditions in winter, good weather in summer, and even on which day of Animals 2021, 11, 611 13 of 18

during the fattening period [12]. One Spanish study, with 60 G males under a fattening intensive system and slaughtered at 15 months reported 1300–1520 g/day [27]. Another study also carried out in Spain and under intensive fattening systems, with approximately 80 bulls per breed studied, also reported higher ADG for G (1370 g/day), A (1250 g/day) and S (1290 g/day) than BA males’ ADG [4]. BAxL males averaged 60.03 ± 2.33% of meat yield while BA males never reached 60% (59.24 ± 2.19%). In females, BAxL had Animals 2021, 11, x 58.08 ± 2.49% while BA never reached 58% (57.05 ± 2.30%) (Figure 11A,B). Although these 13 of 19 were slightly lower percentages than similar breeds adapted to the pasture-based mountain areas such as BP, G or A [4–6,27] and very similar with S breed (58.5%) [4], this result seems logical because the priority of the BA genetic program is maternal aptitude more than meat theperformance. week the Itholidays must be are highlighted in neighboring that comparison countries with (France other studiesand Spain). should All be of carried these factors haveout carefully an effect because on the fattening demand systems for meat, and ageespecially at slaughter in hotels can be and different restaurants and affect in the Andorra, andparameters are different under study.between years.

A 700

600

500

400

300 200 100 0 Body Body weight at slaughter (kg) 07 10 12 13 15 18 20 0 009 0 0 0 0 017 0 0 2 20082 2 20112 2 20142 20162 2 20192

B 700

600

500

400

300 200 100 0 Body Body weight at slaughter (kg) 07 10 12 13 15 18 20 0 009 0 0 0 0 017 0 0 2 20082 2 20112 2 20142 20162 2 20192

Figure 9. Body weight at slaughter from BA (A) and BAxL (B) split by males (blue filled circles) and Figure 9. Body weight at slaughter from BA (A) and BAxL (B) split by males (blue filled circles) females (red filled squares) from 2007 to 2020 in Andorra. Males had higher BW at slaughter than and females (red filled squares) from 2007 to 2020 in Andorra. Males had higher BW at slaughter females in both BA and BAxL groups (p < 0.001) without observing a significant trend across the than females in both BA and BAxL groups (p < 0.001) without observing a significant trend across study period (p > 0.05). the study period (p > 0.05).

Both genders of the BAxL crossbreed showed a significant improvement along the period regarding the ADG and meat yield (p < 0.001) and had better performance during the fattening process than BA animals (p < 0.001) (Figure 10A,B). On average, BA males had an ADG of 1277 ± 175 and females 1031 ± 156 g/day. In BAxL males, the ADG was 1305 ± 175 g/day and BAxL females averaged 1070 ± 152 g/day (see Table S2 in Supple- mentary Materials for yearly detailed results). In contrast, both genders of the BA pure breed showed a slight but significant decrease (p < 0.05) of ADG along the period. This decrease in BA ADG might be explained because the project priority was the maternal characteristics and a better calving ease for the pure breed. The fact that discarded animals as breeders have been finally slaughtered at older ages might also penalize the BA ADG. The ADG in pure BA are lower than those reported in similar breeds such as BP, where 74 BP bulls had an ADG of 1630 g/day [5] or PA, officially reporting 1750 g/day in males during the fattening period [12]. One Spanish study, with 60 G males under a fattening intensive system and slaughtered at 15 months reported 1300–1520 g/day [27]. Another Animals 2021, 11, x 14 of 19

study also carried out in Spain and under intensive fattening systems, with approximately 80 bulls per breed studied, also reported higher ADG for G (1370 g/day), A (1250 g/day) and S (1290 g/day) than BA males’ ADG [4]. BAxL males averaged 60.03 ± 2.33% of meat yield while BA males never reached 60% (59.24 ± 2.19%). In females, BAxL had 58.08 ± 2.49% while BA never reached 58% (57.05 ± 2.30%) (Figure 11A,B). Although these were slightly lower percentages than similar breeds adapted to the pasture-based mountain ar- eas such as BP, G or A [4–6,27] and very similar with S breed (58.5%) [4], this result seems logical because the priority of the BA genetic program is maternal aptitude more than

Animals 2021, 11, 611 meat performance. It must be highlighted that comparison with other studies should14 of be 18 carried out carefully because fattening systems and age at slaughter can be different and affect the parameters under study.

A 1600 1500 1400 1300 1200 1100 1000 900 800 700 350

Average daily Average gain daily (g/day) 0 8 2 6 0 2 00 01 01 20072 2009201020112 2013201420152 20172018201920

B 1600 1500 1400 1300 1200 1100 1000 900 800 700 350

Average daily Average gain daily (g/day) 0 8 2 6 0 2 00 01 01 20072 2009201020112 2013201420152 20172018201920

Figure 10. A B Figure 10. AverageAverage daily daily gain gain (g/day) (g/day) from from BA BA (A ( ) )and and BAxL BAxL (B () )split split by by males males (blue (blue filled filled circles) circles) andand females females (red (red filled filled squares) squares) from from 2007 to 2020 in Andorra. Both genders of the BAxL crossbreedcross- breedimproved improved regarding regarding ADG ADG across across the yearsthe years (p < (p 0.001) < 0.001) and and had had a bettera better performance performance during during the thefattening fattening process process than than BA BA animals animals (p < (p 0.001). < 0.001). However, However, both both genders genders of the of the BA BA pure pure breed breed showed showeda slight a but slight significant but significant decrease de increase ADG in across ADG the across years the (p years< 0.05). (p < 0.05).

The carcass quality of the slaughtered animals was monitored with the SEUROP score and began in 2007. No significant differences have been observed between females and males or between BA and BAxL across the study. Since 2009, the percentage of animals classified as ≥R score has been over 95%. Of special interest is to remark the rapid increase in the percentage of BA animals with ≥R score. In 2007, there was only >75% with ≥R score in both BA females and males and this value has reached >95% since 2009. On the other hand, L pure breed animals usually record >95% with ≥U score [25]. Thus, a better carcass quality would be expected for BAxL versus BA animals, but this is not the case. There is the possibility that the crossbreeding with a less performed breed such as BA, the voluntary avoidance of the muscular hypertrophy gene, and the Andorran harsh conditions reduce the carcass quality of the BAxL compared to the pure L carcass and meat quality are strongly affected not only by the breed, but also by the production system [26,28]. Thus, comparison with other studies is difficult because breed characteristics and production systems are different. However, the fact that the PA official site [12] reports E and U as the most common carcass classification should indicate that there is margin to improve carcass quality in BA. Animals 2021, 11, x 15 of 19 Animals 2021, 11, 611 15 of 18

A 65

60

55

% Meat yield Meat % 50 40 20 0 2 7 07 09 10 11 14 15 16 19 20 0 0 0 20 20082 20 20 201 20132 20 20 201 20182 20

B 65

60

55

% Meat yield Meat % 50 40 20 0 8 2 7 0 1 13 1 18 007 0 010 011 0 0 015 016 0 0 020 2 2 20092 2 2 2 20142 2 2 2 20192

Figure 11. Percentage of meat yield in slaughtered calves from BA (A) and BAxL (B) split by males Figure(filled 11. circles) Percentage and females of meat (filled yield squares) in slaughtered from 2007 calves to from 2020 BA in Andorra.(A) and BAxL Both ( gendersB) split by of males BAxL (filledcrossbreed circles) improved and females across (filled the squares) years regarding from 2007 to meatto 2020 yield in Andorra. (p < 0.001) Both whereas genders this of parameterBAxL crossbreeddoes not show improved any significant across the change years regarding across the to years meat for yield both (p genders < 0.001) of whereas BA (p > this 0.05). parameter does not show any significant change across the years for both genders of BA (p > 0.05). 3.3. Calving Ease and Reproductive Characteristics of the Breed TheSince carcass the start quality of the of program, the slaughtered calving ease animals was one was of themonitored most important with the parameters SEUROP scoreto control. and began The proportion in 2007. No of significant dystocia has differences been continuously have been below observed 8% (scores between CE3 females and 4) andduring males the or whole between period BA under and BAxL study, across except the in 2009study. when Since it was2009, 12.51%. the percentage We did not of ani- find malsany reasonclassified to explainas >R score this punctualhas been increaseover 95%. in Of dystocia special (see interest Table is S2to inremark Supplementary the rapid increaseMaterials, in the available percentage data sinceof BA 2008) animals and with is in >R accordance score. In 2007, with there similar was local only or >75% European with >Rbreeds score adapted in both toBA similar females conditions and males [22 and,24, 29this]. Thisvalue goal has has reached been achieved>95% since because 2009. On the thegenetic other program hand, L always pure breed considered animals a better usually maternal record aptitude>95% with of the>U cowsscore(anatomy [25]. Thus, and a betterbehavior), carcass the quality eradication would of be muscle expected hypertrophy for BAxL (Mh/Mh)versus BA in animals, BA bulls, but and this a reductionis not the case.of BW There at birth is the (Table possibility S2 in Supplementarythat the crossbreeding Materials). with Thea less proportion performed of breed bulls thatsuch areas BA,not the carriers voluntary for Mh avoidance (+/+) has of beenthe muscular increasing hypertrophy across the years,gene, and from the 66.6% Andorran (6/9) harsh in the conditionsyear 2000 toreduce 96.3% the (52/54) carcass in quality 2020 (see of Tablethe BAxL S1 in compared Supplementary to the Materialspure L carcass for yearly and meatdata). quality Thus, are farmers strongly increased affected the not use only of by BA the bulls breed, in substitutionbut also by the of production L bulls for system mating [26,28].heifers Thus, without comparison any negative with impact other studies on calving is difficult ease. Although because breed the eradication characteristics of Mh and in productionthe BA breed systems may penalize are different. in terms However, of fattening the fact efficiency that the (lower PA official meat site yield [12] and reports carcass E quality) [30], the main goal of the genetic program was to increase the number of BA Animals 2021, 11, 611 16 of 18

breeders in order to avoid inbreeding and to have a breed very well adapted to a high mountainous grazing area with limited resources and harsh conditions (climatology and altitude). Although the database provides calving ease scores since 2005, scoring began being systematically recorded in 2008. Since then, the average percent of dystocia (scores CE3 and 4) has significantly dropped from 7% at the beginning of the project (2007–2011) to <3% for the last five years (2016–2020) (p < 0.001). The age at first calving, the average number of parturitions per cow and interval calving–calving were also studied in order to evaluate reproduction performance [31] and decipher if some of these parameters could improve the system and make it more efficient. The average age at first calving was 35.6 ± 5.8 months of age, the average number of parturitions was 4.47 ± 3.08, and interval calving–calving was 13.8 ± 3.9 months. These values are slightly higher but in accordance than the ones reported in similar local breeds, such as BP or PA with ~33 and 32 months at first calving or ~13 and 12.8 months of interval calving–calving, respectively [12,16,32]. The value for the age at first calving in other European breeds, adapted to pastures in the Pyrenees, such as L (33.7 months) or G (31–34 months) was lower than the valued described for BA. [7,33]. While there were no significant differences between years, the three parameters tended to improve (Table S2 in Supplementary Material). We believe that we must be very careful in attributing changes in these parameters to BA cows and their genetic improvement, as a very important limiting factor is the ancestral opinion of farmers, who have always set an age in the first parturition of a cow at 36 months. We consider that a decrease in the age at first parturition should be set as a goal for the next future without any supplementary risk of dystocia, since very similar breeds set 30–33 months of age as a gold standard [12,16,32]. The reduction of the age at first parturition would help in maximizing the efficiency of the Andorran cow–calf farming system.

3.4. Slaughter and Meat Products From the beginning of the project until today, Andorra’s national slaughterhouse has been the only slaughterhouse authorized to slaughter cattle with the label CQCA/IGO Carn d’Andorra. The distribution and marketing of meat has varied over the years. Initially, meat sales went through a meat wholesaler who managed sales in both butchers and restaurants (2000–2010). Afterwards, RASA decided to directly distribute the meat to butchers and restaurants. During the first 10 years of the project (2000–2010), the number of butchers and restaurants that sold CQCA products was variable and the authors of this work have not been able to obtain exact data. During the last ten years, RASA directly distributes the meat to 20 butchers (six of them located in supermarkets), three secondary meat distributors, three catering centers, one hospital, one school, and a health center. Since 2015, one of the secondary distributors (Poltrand-www.poltrand.ad. Accessed on 29 September 2020) has also been offering direct online sales of CQCA products. In an effort to maximize the consumption of CQCA products and maximize the sustainability of the production system, RASA is making many efforts to promote the consumption of parts of the carcass considered second category in the commercial circuit. This promotion is carried out with the incorporation of a butcher and a cook in charge of explaining and promoting ways of consuming and cooking these second category meat and viscera pieces.

4. Conclusions Pasture-based livestock farming with local breeds can generate income in regions with limited resources and harsh conditions, and is a key point to the biodiversity conservation of the area. The project of the BA cow breed has shown that it is possible to bet on local productive systems adapted to the natural resources of the environment. The products obtained from these production systems can take place in a local market where farmers and consumers are able to appreciate the values of the cow–calf grazing system with a local breed, even if this means worse production parameters, meat yield, or a higher price Animals 2021, 11, 611 17 of 18

compared to other farming and marketing systems. A low inbreeding risk, population, and maternal aptitude in the BA breed seem guaranteed. The BA breed can, and should, make efforts in order to improve the age at first calving, fattening efficiency, and carcass quality. However, we believe that these projects need long-term governmental and private cooperation in all the areas to achieve the goals and be successful.

Supplementary Materials: The following are available online at https://www.mdpi.com/2076-261 5/11/3/611/s1, Table S1: Descriptive results of the population of Bruna d’Andorra (BA) and Bruna d’Andorra crossbreed with Limousin (BaxL) during the last twenty-one years (2000–2020), Table S2: Reproductive and productive data of Bruna d’Andorra (BA) and Bruna d’Andorra crossbreed with Limousin (BaxL) population during the last twenty-one years (2000–2020). Author Contributions: R.A. and L.F. conceptualized the design of the study. R.A. and M.B. per- formed the data compilation. L.F. performed the data analysis and R.A. and L.F. interpreted the findings. R.A. and L.F. drafted and reviewed the manuscript. The final approval of the version to be submitted for publication was conducted by R.A. and L.F. All authors have read and agreed to the published version of the manuscript. Funding: This work was not supported by any research project. Acknowledgments: We are very grateful to the owners and farmers (APRA and RASA) for their interest in explaining the traditional system and modern adaptations, to the Govern d’Andorra (GA) Agricultural and Livestock Department, specially to Josep M. Casals, Consòl Naudí, Eduard Torres and Gerard Martínez who helped us so much in the compilation of crucial information for this manuscript. We are also thankful to the English Editor who revised this document. Conflicts of Interest: The authors declare no conflict of interest.

References 1. O’Rourke, E.; Charbonneau, M.; Poinsot, Y. High nature value mountain farming systems in Europe: Case studies from the Atlantic Pyrenees, France and the Kerry Uplands, Ireland. J. Rural Stud. 2016, 46, 47–59. [CrossRef] 2. Zuliani, A.; Contiero, B.; Schneider, M.K.; Arsenos, G.; Bernués, A.; Dovc, P.; Gauly, M.; Holand, Ø.; Martin, B.; Morgan-Davies, C.; et al. Topics and trends in Mountain Livestock Farming research: A text mining approach. Animal 2020, 15, 100058. [CrossRef] 3. Rouzaud, F.; Martin, J.; Gallet, P.F.; Delourme, D.; Goulemote-Leger, V.; Amigues, Y.; Ménissier, F.; Levéziel, H.; Julien, R.; Oulmouden, A. A first genotyping assay of French cattle breeds based on a new allele of the extension gene encoding the melanocortin-1 receptor (Mc1r). Genet Sel. Evol. 2000, 32, 511–520. [CrossRef] 4. Piedrafita, J.; Quintanilla, R.; Sañudo, C.; Olleta, J.L.; Campo, M.M.; Panea, B.; Renand, G.; Turin, F.; Jabet, S.; Osoro, K.; et al. Carcass quality of 10 beef cattle breeds of the Southwest of Europe in their typical production systems. Livest. Prod. Sci. 2003, 82, 1–13. [CrossRef] 5. Serra, X.; Gil, M.; Gispert, M.; Guerrero, L.; Oliver, M.A.; Sañudo, C.; Campo, M.M.; Panea, B.; Olleta, J.L.; Quintanilla, R.; et al. Characterisation of young bulls of the Bruna dels Pirineus cattle breed (selected from old Brown Swiss) in relation to carcass, meat quality and biochemical traits. Mea tSci. 2004, 66, 425–436. [CrossRef] 6. Tarrés, J.; Casellas, J.; Piedrafita, J. Genetic and environmental factors influencing mortality up to weaning of Bruna dels Pirineus beef calves in mountain areas. A survival analysis. J. Anim. Sci. 2005, 83, 543–551. [CrossRef][PubMed] 7. Guerrero, A.; Sanudo, C.; Mateas, J.A.; Caillaud, S.; Sepulveda, W.S.; Toustou, J.; Gajan, J.P.; Santolaria, P. Gasconne Beef Breed, an Explorative Study of Trans-Border Differences in Management and Commercialization. Iran. J. Appl. Anim. Sci. 2012, 3, 257–364. 8. Servei Meteorològic Nacional d’Andorra. Available online: https://www.meteo.ad/climatologia (accessed on 29 September 2020). 9. Servei d’Estadística Nacional d’Andorra. Available online: http://www.estadistica.ad/serveiestudis/publicacions/Publicacions/ Andorra%20en%20Xifres_cat.pdf (accessed on 29 September 2020). 10. APRA. Associació de Pagesos i Ramaders d’Andorra. Available online: https://www.apra.ad (accessed on 7 September 2020). 11. BOPA. Butlletí Oficial del Principat d’Andorra. Available online: https://www.bopa.ad (accessed on 29 September 2020). 12. Asociación de criadores de la raza Parda de Montaña. Available online: https://pardademontana.com/produccion (accessed on 16 December 2020). 13. Jordi Carreras, J.; Carrillo, E.; Font, X.; Guardiola, M.; Ninot, J.M.; Masalles, R.M.; Mercadal, G.; Salvat, A.; Vilar, L.L. Volum V 3 Vegetació arbustiva i herbàcia (Prats i pastures). In Manual dels hàbitats de Catalunya; 2016 Revised; Carreras, J., Ferré, A., Vigo, J., Eds.; Departament de Territori i Sostenibilitat: Generalitat de Catalunya, Barcelona, 2016; Volume 3, pp. 1–234. 14. Komac, B.; de la Parte, I.; Riba, L.; Pladevall, C.; Fanlo, R.; Roquet, M. Pastures Comunes i Ramaderia a Andorra: Usos, gestió i perpectives. In Monografies del CENMA; Komac, B., Pladevall, C., Eds.; Institut d’Estudis Andorrans- Govern d’Andorra: Andorra la Vella, Andorra, 2020. Animals 2021, 11, 611 18 of 18

15. Departament d’Agricultura, Ministeri de Medi Ambient, Agricultura i Sostenibilitat, Govern d’Andorra. Available online: https://www.agricultura.ad/igp (accessed on 3 September 2020). 16. FEBRUPI. Federació Raça Bruna dels Pirineus. Available online: http://www.brunadelspirineus.org (accessed on 7 September 2020). 17. Armengol, R.; Pabón, M.; Santolaria, P.; Cabezón, O.; Adelantado, C.; Yániz, J.; López-Gatius, F.; Almería, S. Low seroprevalence of Neospora caninum infection associated with the Limousin breed in cow-calf herds in Andorra, Europe. J. Parasitol. 2007, 95, 1029–1032. [CrossRef] 18. Classification of Carcasses of Bovine Animals Aged Eight Months or More, European Comission. Available online: https: //ec.europa.eu/info/sites/info/files/food-farming-fisheries/farming/documents/methodology-carcase-remainders_en.pdf (accessed on 20 October 2020). 19. Fina, M.; Ibáñez-Escriche, N.; Piedrafita, J.; Casellas, J. Canalization analysis of birth weight in Bruna dels Pirineus beef cattle. J. Anim. Sci. 2013, 91, 3070–3078. [CrossRef][PubMed] 20. Cañas-Álvarez, J.J.; Gónzalez-Rodríguez, A.; Martín-Collado, D.; Avilés, C.; Altarriba, J.; Baro, J.A.; De la Fuente, L.F.; Díaz, C.; Molina, A.; Varona, L.; et al. Monitoring changes in the demographic and genealogical structure of the main Spanish local beef breeds. J. Anim. Sci. 2014, 92, 4364–4374. [CrossRef] 21. Villalba, D.; Casasús, I.; Sanz, A.; Estany, J.; Revilla, R. Preweaning growth curves in Brown Swiss and Pirenaica calves with emphasis on individual variability. J. Anim. Sci. 2000, 78, 1132–1140. [CrossRef] 22. Bureš, D.; Bartoˇn,L.; Zahrádková, R.; Teslík, V.; Fiedlerová, M. Calving difficulty as related to body weights and measurements of cows and calves in a herd of Gascon breed. Czech J. Anim. Sci. 2008, 53, 187–194. [CrossRef] 23. Krupa, E.; Oravcová, M.; Polák, P.; Huba, J.; Krupová, Z. Factors affecting growth traits of beef cattle breeds raised in . Czech J. Anim. Sci. 2005, 50, 14–21. [CrossRef] 24. Pilarczyk, R.; Wójcik, J. Comparison of calf rearing results and nursing cow performance in various beef breeds managed under the same conditions in north-western . Czech J. Anim. Sci. 2007, 52, 325–333. [CrossRef] 25. Comerford, J.W.; Bertrand, J.K.; Benyshek, L.L.; Johnson, M.H. Reproductive rates, birth weight, calving ease and 24-h calf survival in a four-breed diallel among Simental, Limousin, Polled Hereford and Brahman beef cattle. J. Anim. Sci. 1987, 64, 65–76. [CrossRef] 26. The Beef Site. Available online: https://www.thebeefsite.com/breeds/beef/39/limousin/ (accessed on 16 November 2020). 27. Miranda-de la Lama, G.C.; Pascual-Alonso, M.; Guerrero, A.; Alberti, P.; Alierta, S.; Sans, P.; Gajan, J.P.; Villarroel, M.; Dalmau, A.A.; Velarde, A.; et al. Influence of social dominance on production, welfare and the quality of meat from beef bulls. Meat Sci. 2013, 94, 432–437. [CrossRef] 28. Gil, M.; Serra, X.; Gispert, M.; Oliver, M.A.; Sañudo, C.; Panea, B.; Olleta, J.L.; Campo, M.; Oliván, M.; Osoro, K.; et al. The effect of breed-production in the myosin heavy chain 1, the biochemical characteristics and the colour variables of Longissimus thoracis from seven Spanish beef cattle breeds. Meat Sci. 2001, 58, 181–188. [CrossRef] 29. Tarres, J.; Fina, M.; Piedrafita, J. Parametric bootstrap for testing model fitting of threshold and grouped data models: An applica- tion to the analysis of calving ease of Bruna dels Pirineus beef cattle. J. Anim. Sci. 2010, 88, 2920–2931. [CrossRef] 30. Fiems, O. Double muscling in cattle: Genes, Husbandry, Carcasses and Meat. Animals 2012, 2, 472–506. [CrossRef] 31. Larsson, B.; Berglund, B. Reproductive performance in cows with extended calving interval. Reprod. Domest. Anim. 2000, 35, 277–279. [CrossRef] 32. La vaca Bruna dels Pirineus. Available online: http://agricultura.gencat.cat/web/.content/07-ramaderia/produccio-ramadera/ races-autoctones/enllacos-documents/fitxers-binaris/vaca-bruna-pirineus.pdf (accessed on 16 December 2020). 33. Dákay, I.; Márton, D.; Bene, S.; Kiss, B.; Zsuppán, Z.; Szabo, F. The age at first calving and the longevity of beef cows in Hungary. Arch. Tierz. 2006, 49, 417–425. [CrossRef]