Reproduction in Domestic Animals

Follicular and Oocyte Competence under Heat Stress 239The endocrine background governing alterations infollicular dynamics and depression of dominance underheat stress is not fully understood. Accumulatingevidence indicates alterations in systemic gonadotropin,inhibin and steroid concentrations, as well as in steroidogenesis(for review, see Wolfenson et al. 2000). Heatinducedincreases in the number of medium-sizedfollicles (i.e. immediate effect) were associated withincreased concentrations of follicle-stimulating hormone(FSH) and reduced concentrations of inhibin in theplasma (Wolfenson et al. 1995; Roth et al. 2000a).Inhibin and oestradiol synergistically affect FSH secretion(Kaneko et al. 1995). Thus, heat-induced impairmentof granulosa cell function, the main source ofplasma oestradiol and inhibin, can lead to increasedFSH concentrations in the plasma (Roth et al. 2000a).Follicular steroid production under heat stressSeasonal studies report that lower steroid concentrationsin the follicular fluid obtained from large folliclesduring the hot season are associated with reducedviability of granulosa cells and impaired aromataseactivity (Badinga et al. 1993; Wolfenson et al. 1995).Bridges et al. (2005) reported that follicle piecesobtained from heat-stressed cows secrete lower levelsof androstenedione and oestradiol upon gonadotropinstimulation. Similarly, thecal cells incubated at hightemperatures or collected from heat-stressed cows produceless androstenedione when stimulated by LH, butnot by forskolin, implying a disruption in LH receptorfunction upon heat stress (Wolfenson et al. 1995; Rothet al. 2001b). Nonetheless, expression of the mRNAencoding LH receptors in bovine thecal cells did notprovide evidence of such alterations (Roth et al. 2000b).In contrast, a recent study in goat reported decreasedexpression of LH receptors in heat-stressed follicles(Ozawa et al. 2005). Thus, many aspects of the molecularand cellular mechanisms underlying heat-induceddisruption of steroidogenesis remain to be elucidated.Alterations of steroidogenic capacity induced bysummer heat stress carry over to the final stage offollicle development, as evidenced by reduced androstenedioneproduction by thecal cells and low oestradiolconcentrations in follicular fluid collected from dominantfollicles in the autumn (Wolfenson et al. 1997). Inagreement with this, decreased oestradiol and androstenedioneproduction was recorded in granulosa andthecal cells obtained from follicles three to four weeksafter acute heat stress (Roth et al. 2000a). Similarly,oestradiol content in the follicular fluid aspirated fromcows was relatively low in late summer and increasedthroughout the autumn (Roth et al. 2004). Thus theextent of the heat stress effects on follicular function istransient as also reflected by the spontaneous improvementof fertility throughout autumn and early winter(Zeron et al. 2001).A strategy to enhance the removal of impairedfollicles and the reappearance of apparently normalfollicles was suggested: induction of frequent follicularwaves by hormonal treatment (i.e. GnRH followed byPGF2a (counteracted the effect of summer heat stress(Guzeloglu et al. 2001). Apparently, stimulation ofgonadotropins by GnRH has a beneficial effect ondeveloping follicles since induction of frequent follicularwaves during the autumn increased oestradiol content inpre-ovulatory follicles aspirated from previously heatstressedcows (Roth et al. 2004).Among the potential adverse effects associated withlow oestradiol levels are impairment of oestrus durationand intensity, increased incidence of anoestrus, silentovulation, and a reduced number of mounts (Gwazdauskaset al. 1981). Poor oestrus detection can beimproved by using modern aids such as the Heat-Watchsystem, a radio-telemetric pressure transducer, pedometricoestrus detection or alternatively, utilization ofovulation-synchronization protocols with fixed-timeartificial insemination (AI) procedures (Moore andThatcher 2006). Nevertheless, these procedures cannotovercome the negative effects of heat stress onconception.Reduced oestradiol concentrations in the blood duringthe follicular phase may also affect the pre-ovulatoryLH surge which, in turn, disrupts the cascade of eventsleading to oocyte ovulation. This is demonstrated by thelow amplitude of the GnRH-induced LH surge in heatstressedcows expressing low oestradiol concentration(Gilad et al. 1993). Nonetheless, studies in which GnRHwas administered at the onset of oestrus (Ullah et al.1996; Kaim et al. 2003) increased conception rates inheat-stressed primiparous cows, but this increase wasless pronounced in multiparous cows.Heat Stress and Oocyte DevelopmentalCompetenceIn-vivo and in-vitro studies support the view that bovineoocytes are susceptible to thermal stress at variousstages of follicular development. Perturbation in thephysiology of the follicle-enclosed oocyte during thelengthy period of follicular development could potentiallylead to an oocyte with reduced competence forfertilization and subsequent development.Oocytes harvested from cows during the summerexhibit a reduced ability to develop to the blastocyststage after in-vitro fertilization (Rocha et al. 1998; Al-Katanani et al. 2002) or chemical activation (Zeronet al. 2001). Cleavage to the two- and four-cell stagesfollowing chemical activation was delayed in bovineoocytes collected during the hot season (May–November)relative to oocytes collected during the cold season(December–April) (Aroyo et al. 2007b). The timing offirst cleavage (early vs delayed) is considered to havemajor long-lasting effects on subsequent embryonicdevelopmental potential (Fenwick et al. 2002), whichmay explain the inferior developmental competence ofoocytes collected during the summer.Elevated air temperatures before oestrus have beenassociated with reduced fertility (Al-Katanani et al.1999; Chebel et al. 2004). Intensive cooling from 1 daybefore oestrus to 8 days post-AI did not improve theconception rate of cows in the summer (Her et al. 1988).Similarly, using a fan-and-fogger cooling system 42 daysbefore oocyte collection did not increase the proportionof oocytes that developed to the blastocyst stage (Al-Katanani et al. 2002). Thus, either the oocytes wereÓ 2008 The Author. Journal compilation Ó 2008 Blackwell Verlag