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Small Ruminant Research 90 (2010) 161–164

Contents lists available at ScienceDirect

Small Ruminant Research

journa l homepage: www.e lsev ier .com/ locate /smal l rumres

hort communication

ocial ranking and plasma progesterone levels in goats

. Alvarez ∗, R.R. Arvizu, J.A. Luna, L.A. Zarcoacultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Ciudad de México, 14500, Mexico

r t i c l e i n f o

rticle history:eceived 29 September 2009eceived in revised form 5 February 2010ccepted 8 February 2010vailable online 3 March 2010

eywords:ocial dominancerogesterone valuesoatsarly gestationeproduction

a b s t r a c t

Progesterone is essential for maintaining pregnancy in goats, and embryonic losses maybe a consequence of the reduction in circulating progesterone levels close to the time ofimplantation. Some evidence exists regarding social dominance affecting the plasma pro-gesterone levels in several species—where dominant females conceive earlier. The objectiveof this research was to determine whether serum progesterone levels differ in goats of dif-ferent social status. A behavioural study was conducted for 10 days in a herd of 57 does andan individual success index (SI) was calculated according to the result of aggressive inter-actions. Goats were classified as high (SI: 1–0.67), medium (SI: 0.66–0.34) and low-ranking(SI: 0.33–0.0). Ovulation was synchronized using two injections of prostaglandin 11 daysapart, and the plasma progesterone levels determined daily for a period of 20 days. The areaunder the plasma progesterone curve during the entire study was greater in the high than in

the medium and low-ranking does (96.2 ± 5.8, 79.5 ± 5.3 and 81.3 ± 5.3 ng/ml, respectively,P < 0.05). During days 11–17 following prostaglandin synchronization, the plasma proges-terone levels were higher in the high-ranking (P < 0.05), compared to the low-ranking does.Plasma progesterone levels were significantly correlated with SI at days 14 and 15 (r = 0.26;P < 0.05). Results suggest a relationship between social ranking of goats and the plasma

uction

progesterone prod

. Introduction

In goats, pregnancy recognition occurs between day3 (Jarrell and Dziuk, 1991) and 17 (Gnatek et al., 1989)ollowing mating. As in other mammals, the initial estab-ishment of pregnancy depends on progesterone secretiony the corpus luteum, which is necessary for success-ul implantation (Vincent and Inskeep, 1986). In many

ituations, embryonic loss may be related to an inade-uate production of progesterone by the corpus luteumInskeep, 2004), close to the time of implantation (Bazert al., 1994). In some experiments, attempts to improve

∗ Corresponding author at: Departamento de Producción Animal,acultad de Medicina Veterinaria y Zootecnia, Av. Universidad #3000, Del-gación Coyoacán, Ciudad Universitaria, Ciudad de México, Mexico.el.: +52 55 58 48 05 15; fax: +52 55 58 48 05 14.

E-mail addresses: alorenzo@unam.mx,orenzoalvarezramirez@gmail.com (L. Alvarez).

921-4488/$ – see front matter © 2010 Elsevier B.V. All rights reserved.oi:10.1016/j.smallrumres.2010.02.002

from the corpus luteum and other possible sources.© 2010 Elsevier B.V. All rights reserved.

conception rates have included exogenous progesteroneadministration (Borque et al., 1993; Lopez-Gatius et al.,2004; Alnimer and Lubbadeh, 2008), or luteotrophin sup-plementation during early pregnancy (Kerbler et al., 1997;Nishigai et al., 2002). Progesterone treatment immediatelyfollowing ovulation has been shown to increase the con-ception rate in cattle (Robinson et al., 1989; Binelli et al.,2001) and improve embryo quality in does (Akinlosotu andWilder, 1993).

Social interactions affect reproductive function in awide range of species. A sub-ordinate social status gen-erally leads to suppressed or delayed estrous behaviourin goats (Alvarez et al., 2003), cows (Orihuela, 2000) andsows (Pedersen et al., 2003), as well as delayed ovulation in

goats (Abbott et al., 1981; Alvarez et al., 2003, 2009). It hasalso been reported that social ranking influences ovarianendocrine activity immediately after conception in red deerhinds (Cervus elaphus). Serum progesterone concentrationshave also been shown to be greater in high-ranking than in

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low-ranking females after ovulation (Flint et al., 1997). Inred deer it has also been reported that dominant hinds con-ceive earlier in the breeding season than their low-rankingherd-mates (Clutton-Brock et al., 1986).

Thus high-ranking does presumably ovulate and con-ceive earlier, and a greater proportion of the femalesdisplay estrous behaviour, compared to counterparts inthe herd (Alvarez et al., 2003, 2007). However, the rela-tionship between social ranking and plasma progesteroneconcentrations has not been studied in does. This study wasthus conducted to determine the relationship between thesocial ranking in a group of female goats and their plasmaprogesterone concentrations.

2. Materials and methods

2.1. Animal management and behavioural recordings

The study was conducted at an experimental farm located in Mex-ico City (Mexico). During November (late autumn), 57 Creole does werehoused in two 160 m2 pens (n = 28 and 29, respectively). Aggressivebehavioural interactions were recorded 5 h per day (10:00 to 13:00 h and14:00 to 16:00 h) for 10 consecutive days in each group of goats (Alvarezet al., 2009).

Behavioural actions included all aggressive interactions includinghead butting; threats (when a goat turned towards or approached anotherindividual, head down and lunged, without making contact); chases(when a goat actively moved towards another individual, causing the lat-ter to walk or run away); and avoidance (when a goat actively movedaway from another individual whether or not previous interaction hadoccurred between the two individuals). The initiator, winner and loser ofeach interaction were recorded and the end of an agonistic interactionwas considered when one of the animals involved, withdrew. From theserecordings, a dominance matrix was created and a success index (SI) foreach goat was calculated according to Galindo and Broom (2000) for dairycows, and later used in goats (Barroso et al., 2000; Ungerfeld et al., 2007;Alvarez et al., 2009):

SI (success index) = number of individua(number of individual goats that a doe is able to disp

The SI of a female thus represents the proportion of other animalswith which that goat had antagonistic interactions that culminated in thefirst doe displacing the last. Does that win all their interactions with theircounterparts were allotted an SI of 1, while animals that lost every inter-action had an SI of 0. Three social rankings were defined according tothe SI of each doe: high (0.67–1.0), medium (0.34–0.66) and low-ranking(0.0–0.33) (Barroso et al., 2000; Galindo and Broom, 2000; Alvarez et al.,2009).

Feeding was daily at 08:00 (oat hay and silage) and 14:00 (concen-trate and alfalfa), according to the requirements of the National ResearchCouncil (NRC, 1981), with free access to water.

2.2. Estrous cycle synchronization, blood sampling and plasmaprogesterone determinations

After behavioural recordings, does were treated with two injections ofa 10 mg prostaglandin (PGF2<alpha>) analogue (Dinoprost trometamine,Lutalyse® , Pharmacia Upjohn® México), 11 days apart. Two days followingthe second PGF injection, and for a period of 20 days, blood samples weretaken daily from all goats using vacutainer tubes, with heparin as anti-coagulant. Samples were centrifuged immediately after collection and theplasma aspirated and frozen at −20 ◦C, until assayed. Plasma progesteroneconcentrations were determined using a solid-phase RIA (Srikandakumaret al., 1986), commercial kit (Diagnostic Products Corporation, Los Ange-les, CA, USA) and a standard curve based on goat serum. The detection limit

of the assay was 0.10 ng/ml, and the intra-assay coefficient of variation5.2%.

Ovulation was considered to have occurred 3 days before the plasmaprogesterone reached a level of 1 ng/ml (de Castro et al., 1999). The plasmaprogesterone levels of every sampling were added to calculate the areaunder the curve (AUC) during the entire study.

hat a doe is able to displaceumber of individual goats that are able to displace the doe)

.

Fig. 1. Plasma progesterone concentrations according to the social rank-ing after the synchronization treatment in does.

2.3. Data analysis

Both groups of goats were considered as one, including the pen as acovariate. A statistical correlation was calculated between the plasma pro-gesterone concentration and the individual SI value (SAS, 1999). The AUCwas compared by an ANOVA. Data were presented as the mean ± S.E.M.Differences with a confidence level of P < 0.05 were considered to be sig-nificant.

3. Results and discussion

No significant effect of the pen on the plasma proges-terone concentrations at any time of the experiment wasrecorded. Twenty does were classified as low-ranking, 20as medium-ranking and 17 as high-ranking in the herd. Alldoes ovulated immediately after the second PGF treatment,with no differences in the intervals to ovulation betweengoats of the 3 social rankings (high: 3.5 ± 0.3 d; medium:

3.5 ± 0.2 d and low: 3.2 ± 0.2 d). This is in agreement withthe lack of effect of social ranking in estrous synchro-nization treatments previously reported (Ungerfeld et al.,2007). In goats, the hierarchical position does not affectthe conception rate and litter size following synchroniza-tion treatment, using medroxiprogesterone acetate andPGF (Ungerfeld et al., 2007). Similarly, in the present exper-iment there were no differences in the response to PGFadministration, probably as the reproductive responses aremaximized when highly effective hormonal treatments areapplied.

The plasma progesterone profiles are set out inFig. 1. The AUC was greater in the high than in themedium and low-ranking does (96.2 ± 5.8, 79.5 ± 5.3 and81.3 ± 5.3 ng/ml, respectively; P < 0.05). The highest con-centrations of plasma progesterone were related to SI’s atdays 14 and 15 (r = 0.26; P < 0.05, Fig. 2). This is in agreementwith previous reports in other ruminants like, e.g. the reddeer (Flint et al., 1997; Goodwin et al., 1998). The higherprogesterone concentrations observed in the high-ranking

does may have been provoked by more intensive secretoryactivity of the corpus luteum, or due to a larger num-ber of corpora lutea (CL’s) close to the time of pregnancyrecognition (Jarrell and Dziuk, 1991). There is evidencethat dominant goats produce more CL’s after a superovu-

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ig. 2. Positive correlation between plasma progesterone and the successndex (r = 0.26, P < 0.05) in does.

ation treatment (Ungerfeld et al., 2007). However, theelationship between social ranking and the number ofL’s after superovulation was observed only during theon-breeding season (Ungerfeld et al., 2007), it should beonsidered that the corpus luteum of high-ranked doesre probably more active than those from medium or low-anked does.

Plasma progesterone concentrations have beeneported to be lower in goats with reduced access to feedAl-Azraqi, 2007). The greater progesterone secretion inominant does may also be associated with better accesso nutritional resources (Flint et al., 1997), as it is knownhat dominant animals show high-priority in obtainingeed (Appleby, 1980; Brouns and Edwards, 1994).

Two steroidogenically active cell types have been iden-ified within the CL, namely small and large luteal cellsDiaz et al., 2002; Hoyer and Niswender, 1985). Large lutealells are derived from the luteinized granulosa cells andave a high basal progesterone production (Meidan et al.,990). A decrease in the number of large luteal cells haseen shown to reduce the circulating progesterone concen-ration in cows (Milvae et al., 1991). A difference in accesso nutritional resources (Gasser et al., 2006; Zarazaga etl., 2005), and a difference in balance of the hypothalamo-onadal axis between dominant and sub-ordinate animalsAlvarez et al., 2007), may induce limited follicle devel-pment, reducing the number of large luteal cells in theub-ordinate does. However, this has yet to be evaluated.

Overall, it can be concluded that progesterone secre-ion during the luteal phase is positively related to theocial dominance in goats. This difference may explain theifferences in conception time between dominant and sub-rdinate does.

cknowledgements

Dr. Rodolfo Ungerfeld is acknowledged for his com-ents and suggestions to the manuscript, and ProjectNAM-DGAPA-PAPIIT IN210006 for funding the study.

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