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Using wireless rumen sensors for evaluating the effects of diet and ambient temperature in nonlactating dairy goats

  • A. Castro-Costa
    Affiliations
    Group of Research in Ruminants (G2R), Department of Animal and Food Sciences, Universitat Autònoma de Barcelona, Bellaterra 08193, Spain
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  • A.A.K. Salama
    Affiliations
    Group of Research in Ruminants (G2R), Department of Animal and Food Sciences, Universitat Autònoma de Barcelona, Bellaterra 08193, Spain

    Sheep and Goat Research Department, Animal Production Research Institute, 12311 Dokki, Giza, Egypt
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  • X. Moll
    Affiliations
    Group of Research in Experimental Surgery and Anesthesiology (GRESA), Department of Animal Medicine and Surgery, Universitat Autònoma de Barcelona, Bellaterra 08193, Spain
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  • J. Aguiló
    Affiliations
    Group of Biomedical Applications (GAB), Department of Microelectronics and Electronic Systems, Universitat Autònoma de Barcelona, Bellaterra 08193, Spain
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  • G. Caja
    Correspondence
    Corresponding author:
    Affiliations
    Group of Research in Ruminants (G2R), Department of Animal and Food Sciences, Universitat Autònoma de Barcelona, Bellaterra 08193, Spain
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Open ArchivePublished:May 07, 2015DOI:https://doi.org/10.3168/jds.2014-8819

      Abstract

      Sixteen Murciano-Granadina dairy goats, provided with wireless rumen sensors for pH and temperature, were used to assess the rumen environment variations produced by extreme forage to concentrate diets (experiment 1) and climatic conditions (experiment 2). To avoid the interference of feed intake, goats were fed at maintenance level. Rumen sensors were inserted by surgery and programmed to collect and store rumen pH and temperature every 30 min. In experiment 1, 8 dry goats (38.6 ± 2.3 kg of body weight) in tiestalls were divided into 2 groups and fed at maintenance level with 2 diets varying in forage-to-concentrate ratio [high forage (HF) 70:30; low forage (LF) 30:70] according to a crossover design. Diets were offered once daily for 4 h and tap water (4 L, 9.8 ± 0.4°C) was offered for only 30 min at 6 h after feeding. Rectal temperatures were recorded 3 times during the day. Rumen pH fell immediately after feeding, reaching a nadir depending on the diet (HF = 6.35 ± 0.07 at 11 h after feeding; LF = 6.07 ± 0.07 at 6 h after feeding) and being on average greater (0.31 ± 0.06) in HF than LF goats. No diet effects were detected in rectal (38.2 ± 0.1°C) and ruminal (38.9 ± 0.1°C) mean temperatures, which were positively correlated. Rumen temperature dramatically changed by feeding (1.4 ± 0.1°C) and drinking (−3.4 ± 0.1°C), and 2 h were necessary to return to the fasting value (38.2 ± 0.1°C). In experiment 2, 8 dry goats (43.9 ± 1.0 kg of body weight) were kept in metabolic cages, fed a 50:50 diet and exposed to 2 climatic conditions following a crossover design. Conditions were thermoneutral (TN; 20 to 23°C day-night) and heat stress (HS; 12-h day at 37°C and 12-h night at 30°C). Humidity (40 ± 5%) and photoperiod (light-dark, 12–12 h) were similar. Goats were fed at maintenance level, the feed being offered once daily and water at ambient temperature was freely available. Intake, rectal temperature, and respiratory rate were recorded 3 times daily. Despite no differing in dry matter intake, rumen pH was lower in HS than in TN goats (−0.12 ± 0.04). On the contrary, rumen temperature (0.3 ± 0.1°C), rectal temperature (0.4 ± 0.1°C), respiratory rate (77 ± 5 breaths/min), and water intake (3.2 ± 0.7 L/d) had a greater increase in HS than TN, which might indicate an altered microbial fermentation under high temperature conditions. In conclusion, wireless bolus sensors proved to be a useful tool to monitor rumen pH and temperature as affected by different feeding and climatic conditions.

      Key words

      Introduction

      Continuous data acquisition by telemetry allows dynamic measuring of responses and helps to define associations with management and environmental variables (
      • Eigenberg R.A.
      • Brown-Brandl T.M.
      • Nienaber J.A.
      Sensors for dynamic physiological measurements.
      ;
      • Rutten C.J.
      • Velthuis A.G.J.
      • Steeneveld W.
      • Hogeveen H.
      Invited review: Sensors to support health management on dairy farms.
      ). Using wireless rumen boluses based on the use of radiofrequency, variation of rumen temperature by estrus and parturition (
      • Cooper-Prado M.J.
      • Long N.M.
      • Wright E.C.
      • Goad C.L.
      • Wettemann R.P.
      Relationship of ruminal temperature with parturition and estrus of beef cows.
      ), viral diarrhea infection (
      • Rose-Dye T.K.
      • Burciaga-Robles L.O.
      • Krehbiel C.R.
      • Step D.L.
      • Fulton R.W.
      • Confer A.W.
      • Richards C.J.
      Rumen temperature change monitored with remote rumen temperature boluses following challenges with Bovine Viral Diarrhea Virus and Mannheimia haemolytica.
      ), SARA (
      • AlZahal O.
      • Steele M.A.
      • Valdes E.V.
      • McBride B.W.
      Technical note: The use of a telemetric system to continuously monitor ruminal temperature and to predict ruminal pH in cattle.
      ), and IMI (
      • AlZahal O.
      • AlZahal H.
      • Steele M.A.
      • Van Schaik M.
      • Kyriazakis I.
      • Duffield T.F.
      • McBride B.W.
      The use of a radiotelemetric ruminal bolus to detect body temperature changes in lactating dairy cattle.
      ) have been reported in cattle.
      Changes in ambient temperature induce different responses in the nervous, circulatory, respiratory, renal, and endocrine systems, which allow the animal to cope with the altered environment. Different physiological, lactational, and nutritional responses to heat stress have been reported in ruminants: by
      • Baumgard L.H.
      • Rhoads R.P.
      Effects of heat stress on postabsorptive metabolism and energetics.
      in dairy cows, and by
      • Hamzaoui S.
      • Salama A.A.K.
      • Albanell E.
      • Such X.
      • Caja G.
      Physiological responses and lactational performances of late lactating dairy goats under heat stress conditions.
      and
      • Salama A.A.K.
      • Caja G.
      • Hamzaoui S.
      • Badaoui B.
      • Castro-Costa A.
      • Façanha D.A.E.
      • Guilhermino M.M.
      • Bozzi R.
      Different levels of response to heat stress in dairy goats.
      in dairy goats. However, little is known about changes in rumen pH and temperature due to heat stress.
      When feed intake was held constant in thermoneutral (TN) and heat stress (HS) environments, HS reduced the concentration of VFA in the rumen of cattle (
      • Kelley R.O.
      • Martz F.A.
      • Johnson H.D.
      Effect of environmental temperature on ruminal VFA levels with controlled feed intake.
      ), increased the concentration of lactic acid, and reduced ruminal pH (
      • Mishra M.
      • Martz F.A.
      • Stanley R.W.
      • Johnson H.D.
      • Campbell J.R.
      • Hilderbrand E.
      Effect of diet and ambient temperature-humidity on ruminal pH, oxidation reduction potential, ammonia and lactic acid in lactating cows.
      ). Moreover, profiling the rumen microbiota by 16s RNA gene cloning confirmed that HS induces significant changes in microbial diversity in heifers, resulting in a decrease of acetate and acetate-to-propionate ratio and an increase of butyrate, which substantially decreases the efficiency of absorption of VFA and the overall rumen pH (
      • Tajima K.
      • Nonaka I.
      • Higuchi K.
      • Takusari N.
      • Kurihara M.
      • Takenaka A.
      • Mitsumori M.
      • Kajikawa H.
      • Aminov R.I.
      Influence of high temperature and humidity on rumen bacterial diversity in Holstein heifers.
      ).
      To our knowledge, telemetry has not been used to continuously measure changes in rumen environment in goats. Therefore, the objective of the present study was to evaluate the use of wireless sensors to assess the ruminal variations produced by diets with different forage-to-concentrate ratios and to monitor the effects of climatic conditions on the rumen environment of nonlactating dairy goats. To avoid confusion between reduced DMI and HS effects, both TN and HS goats were kept at the same level of feed intake to meet maintenance requirements.

      Materials and Methods

      The experimental procedures and animal care conditions were reviewed and approved by the Ethical Committee on Animal and Human Experimentation of the Universitat Autònoma de Barcelona (reference CEEAH 11/1166) and the codes of recommendations for the welfare of livestock of the Ministry of Agriculture, Food and Environment of Spain.

      Wireless Rumen Sensors

      Wireless rumen boluses (model KB1001, Kahne, Auckland, New Zealand), designed for cattle heavier than 300 kg of BW, were used for recording rumen pH and temperature in goats. Measurement ranges for temperature and pH were 0 to 45°C (accuracy = ±0.08°C) and 4.00 to 8.00 (accuracy = ±0.02), respectively. The whole telemetric Khane system included (1) rumen boluses (27 mm diameter × 145 mm height, 70 g weight); (2) magnet blocker, to turn on and off the boluses; (3) top receiver, for capturing the data signals sent by the boluses (frequency = 433.9 MHz); (4) field receiver, with a directional antenna Yagi-Uda type (frequency = 400 to 500 MHz); (5) trigger device, for transmitting the data to the storage device through radio frequency (Kahne wand); and (6) software (Kahne Data Processing System, v.5.2.4), for enabling the configuration and communication between the boluses and transceivers via a computer.
      Boluses were calibrated before use according to the manufacturer instructions (
      • Kahne
      ) using deionized water at 40.0 ± 0.5°C and pH buffer standard solutions of 4.01 and 7.00 (pH25, Crison Instruments, Barcelona, Spain). Measured and reference pH values correlated (R2 = 0.99; P < 0.001). Before the insertion of boluses into the rumen, previously stored data were erased and they were configured to record pH and temperature values every 30 min.
      In vivo validation was conducted using a rumen-cannulated dairy cow fed a maintenance diet (alfalfa hay ad libitum and 3 kg/d of concentrate). Rumen content was sampled beside the bolus sensor at 10 time points (0, 2, 6, 10, and 24 h during 2 d), filtered through a cheesecloth for rumen liquor and pH measured using the previously indicated pH meter, to register extreme pH daily variations.
      Boluses (n = 8) were inserted into the rumen of goats through surgery (
      • Dehghani S.N.
      • Ghadrdani A.M.
      Bovine rumenotomy: Comparison of four surgical techniques.
      ). Goats were fasted for 24 h and were sedated by an i.m. injection of 0.3 mL of xylazine (Rompun 50 mg/mL; Bayer Hispania, Barcelona, Spain) and 1 mL of ketamine (Ketamina 50 mg/mL; Holliday-Scott, Buenos Aires, Argentina) before surgery. After washing, clipping, and disinfecting, a vertical incision of approximately 10 cm was made in the left flank, between the last rib and the iliac tuberosity. After pulling out the rumen wall to the incision with the help of towel clamps, a ruminotomy of 8 cm was done and the bolus was introduced into the rumen with its wings folded and tied to prevent damage to the rumen wall. After suturing the rumen wall, muscle layer, and skin, 2 mL of meloxicam anti-inflammatory (Metacam 20 mg/mL; Boehringer-Ingelheim, Barcelona, Spain) and 4 mL of amoxicillin (Invemox 1.5 mg/mL; Invesa, Barcelona, Spain) were i.m. injected for 5 d. Goats were allowed to recover after surgery for 2 wk in straw-bedded pens and fed alfalfa hay ad libitum.
      A similar surgical procedure was followed to remove the boluses from the rumen at the end of the experiments. With this aim, the goats were lodged in straw-bedded pens and fed alfalfa hay ad libitum for a resting period of 1 wk before surgery. Retrieved rumen sensors were washed with tap water and recalibrated as above indicated to calculate the drift error of the pH and temperature measurements.

      Experiment 1

      Animals, Management, and Treatments

      Eight multiparous (4.5 ± 0.6 yr) nonlactating female Murciano-Granadina goats (38.6 ± 2.3 kg of BW) from the herd of the Experimental Farm of the Servei de Granges i Camps Experiments of the Universitat Autònoma de Barcelona (Bellaterra, Barcelona, Spain) were used. Does were kept indoors in straw-bedded tiestalls at natural temperature and light conditions and individually fed and watered. The experiment was conducted during winter and minimum and maximum ambient temperatures in the barn averaged 10.0 ± 0.4 and 16.2 ± 0.5°C, respectively, throughout the experiment.
      The experimental design was a crossover with 2 treatments in 2 periods (lasting 19 d each) and 4 goats each. Does were switched to the opposite treatment in the second period with a 3-d transitional period to gradually shift to the new diet. Dietary treatments consisted of high- and low-forage-to-concentrate ratio (HF and LF, 70:30 and 30:70, respectively). Dehydrated fescue hay and whole barley grain (see composition in Table 1) were used to formulate the diets that cover the maintenance requirements of dry and open does according to
      INRA
      Alimentation des Bovins.
      . With the aim of identifying the rumen changes produced by feeding and drinking, diets were offered punctually once daily and for 4 h (distributed at 1130 h and withdrawn at 1530 h), whereas tap water (4 L, 9.8 ± 0.4°C) was offered in individual buckets 2 h after feed removal (1730 h) for 30 min. Does had free access to mineral-vitamin blocks in the stall (composition: Na = 36.74%; Ca = 0.32%; Mg = 1.09%; Zn = 5 g/kg; Mn =1.5 g/kg; S = 0.91 mg/kg; Fe = 304 mg/kg; I = 75 mg/kg; Co = 50 mg/kg; Se = 25 mg/kg; Ovi bloc, Sal Cupido, Terrasa, Spain).
      Table 1Chemical composition and nutritive value (DM basis) of the rations
      ItemExperiment 1Experiment 2
      Fescue

      hay
      BarleyAlfalfa

      hay
      Barley
      Component, %
       DM91.791.088.689.5
       OM88.397.187.497.4
       CP10.79.620.010.8
       NDF55.417.736.716.4
       ADF32.55.927.06.1
       NFC
      Fermentable carbohydrates not recovered in NDF, referred to as nonfiber carbohydrates (OM − NDF − CP − fat).
      20.266.828.767.2
      Nutritive value
      Calculated according to INRA (2007).
       UFL/kg
      Feed units for lactation (1 UFL=1.7Mcal NEL).
      0.721.050.721.06
       NEL, Mcal/kg1.221.791.221.80
       PDIE,
      Protein digested in the small intestine supplied by microbial protein from rumen-fermented OM.
      g/kg
      779510198
       PDIN,
      Protein digested in the small intestine supplied by microbial protein from RDP.
      g/kg
      676612874
       PDIA,
      Protein digested in the small intestine supplied by RUP.
      g/kg
      28285632
       Ca, g/kg4.50.816.70.8
       P, g/kg3.04.02.34.0
      1 Fermentable carbohydrates not recovered in NDF, referred to as nonfiber carbohydrates (OM − NDF − CP − fat).
      2 Calculated according to
      INRA
      Alimentation des Bovins.
      .
      3 Feed units for lactation (1 UFL = 1.7 Mcal NEL).
      4 Protein digested in the small intestine supplied by microbial protein from rumen-fermented OM.
      5 Protein digested in the small intestine supplied by microbial protein from RDP.
      6 Protein digested in the small intestine supplied by RUP.

      Sampling, Measurements, and Analyses

      Data were collected during the last 7 d of each experimental period. Samples of feed ingredients were taken at the start of the experiment and diets and orts were daily sampled, composited as representative samples, and stored at 4°C until analysis. Feed intake and water consumption were daily recorded. Samples were ground to pass through a 1-mm stainless steel screen (Cyclotec 1093 Sample mill, Tecator, Höganäs, Sweden) for chemical composition according to
      AOAC International
      . The DM was determined at 103°C for 24 h and samples were burnt thereafter in a muffle furnace at 550°C for 4 h to measure their ash content. Crude protein (N × 6.25) was analyzed according to the Dumas method for N determination using a Leco analyzer (Leco Corporation, St. Joseph, MI). The NDF and ADF were determined using an Ankom200 Fiber Analyzer incubator (Ankom Technology, Macedon, NY) adding α-amylase and sodium bisulfite solutions. Chemical composition and nutritive value of the dietary ingredients are shown in Table 1.
      Daily rectal temperatures were measured at 0900, 1300, and 1700 h using a digital clinical thermometer (Model mini color, ICO Technology, Barcelona, Spain; range = 32.0–43.9°C; accuracy = ±0.1°C). Urine samples were manually collected from each goat when the animals woke up on the last day of each period and pH was measured using a portable pH-meter (pH25, Crison Instruments) within 1 h after collection.

      Experiment 2

      Animals, Management Conditions, and Treatments

      Eight Murciano-Granadina nonlactating does (43.9 ± 1.0 kg of BW; 4.3 ± 0.8 yr) previously adapted (1 wk) to metabolic cages were used. The experimental design was a crossover with 2 treatments in 2 periods lasting 21 d each (adaptation = 14 d; measuring and sampling = 7 d) and 4 goats in each group. Does were switched to the opposite treatment in the second period of 21 d.
      Treatments consisted of different ambient conditions—(1) TN and (2) HS—according to their thermo-hygrometric index [THI = 1.8 × T + 32 – (0.55 − 0.0055 × RH) × (1.8 × T − 26.8), where T is the air temperature and RH is the relative humidity (
      NRC
      A Guide to Environmental Research on Animals. Natl. Acad.
      ); a value of THI >75 was considered as indicative of HS for dairy goats according to
      • Silanikove N.
      Effects of heat stress on the welfare of extensively managed domestic ruminants.
      and
      • Hamzaoui S.
      • Salama A.A.K.
      • Albanell E.
      • Such X.
      • Caja G.
      Physiological responses and lactational performances of late lactating dairy goats under heat stress conditions.
      ]. The TN does were kept in an air-conditioned room (Summit-Serie E10; Hitachi, Barcelona, Spain) maintained between 20 and 23°C with 45% relative humidity (THI = 65–68). The HS does were kept in a climatic chamber (4 × 6 × 2.3 m; ETS Lindgren-Euroshield Oy, Eura, Finland) with temperature and humidity regulation (Carel Controls Iberica, Barcelona, Spain) set to 37°C (from 0900 to 2100 h; THI = 85) and to 30°C (from 2100 to 0900 h; THI = 77). Air turnover (ventilation = 90 m3/h) and relative humidity (RH = 40%) were maintained constant. A 12 and 12 h (light-dark) artificial photoperiod was maintained constant during the experiment in both cases (0900 to 2100 h). When does were switched from TN to HS conditions, a transition period of 2 d was allowed (d 1 at 25°C and d 2 at 30°C) to avoid a thermal shock of the goats, but no transition was applied for the change from HS to TN because of the thermal stress alleviation.
      Goats were fed a diet with 50:50 forage-to-concentrate ratio at maintenance level according to
      INRA
      Alimentation des Bovins.
      . The ration consisted of dehydrated alfalfa hay and barley (see composition in Table 1), the daily ration being individually calculated in accordance with the doe BW and
      INRA
      Alimentation des Bovins.
      requirements. Feed was offered once a day at 1200 h and left for 24 h. Mineralized salt blocks similar to experiment 1 were freely available in each metabolic cage (Ovi bloc, Sal Cupido). Clean water was freely available at ambient temperature for each treatment.

      Measurements, Sampling, and Analyses

      Rectal temperatures and respiration rates were daily recorded at 0900, 1300, and 1700 h. The rectal temperature was measured with the same digital clinical thermometer used in experiment 1. The respiration rate was measured by counting the inhalations and exhalations for 60 s with the aid of a chronometer.
      Feed samples were collected before the beginning of each experimental period and analyzed as in experiment 1. Moreover, orts were daily collected, weighed, and composited for analysis as in experiment 1. All samples were ground through a 1-mm stainless steel screen, and analyzed for DM, CP, ADF, and NDF by adding α-amylase and sodium bisulfite (
      AOAC International
      ).
      Digestibility measurements were done during the last 7-d of each experimental period. Feces were daily collected and 10% of fresh feces were dried at 60°C for 48 h; then a composited sample for each goat was stored at room temperature and processed for analysis as previously indicated. Apparent digestibility (d) of each nutrient was estimated by the expression
      d=(1excreted/ingested)×100.


      Water was freely available at room temperature (individual water tanks in each metabolic cage) and consumption was recorded daily by weight (accuracy = ±20 g) during the digestibility period experiment. Trays with sawdust were put on the floor below the drinking troughs and weighed twice daily to take into account water leaks. Samples of urine were collected at micturition at 0800 and at 1700 h on the last 2 experimental days to measure urine pH.
      With the aim of checking the physiological stage of the goats at the end of the experiment, blood samples (approximately 0.3 mL) were collected before feeding at d 21 of the second period by using insulin syringes (1 mL BD Micro-Fine, BD Medical-Diabetes Care, Franklin Lakes, NJ). A single drop of blood was applied to disposable i-STAT EC8+ cartridges (Abaxis, Union City, CA) for analysis of glucose, urea, Cl, Na, K, total CO2 concentration, anion gap, hematocrit, hemoglobin, pH, partial pressure of CO2, HCO3, and base excess in blood using a VetScan i-STAT 1 hand-held analyzer (Abaxis) programmed for veterinary analysis of small ruminants.

      Statistical Analyses

      Data were analyzed by the PROC MIXED for repeated measurements of SAS version 9.1.3 including the repeated statement (SAS Institute Inc., Cary, NC). The statistical mixed model used for both experiments contained the fixed effects of the treatment (experiment 1 = HF vs. LF; experiment 2 = TN vs. HS), period (1 or 2), sampling time (1 to 48), sequence of treatment (1 or 2), interaction of treatment × sampling time, random effects of the animal (experiment 1 = 1 to 8; experiment 2 = 9 to 16), and residual error. Data of ruminal pH and temperature were averaged for the 7-d measurement period.
      Data of digestibility and blood and urine measures taken in experiment 2 were analyzed by ANOVA using PROC GLM of SAS. The model contained the effects of treatment (TN or HS), period (1 or 2), the sequence of treatment (1 or 2), and the residual error.
      Daily rumen pH and temperature data were used to calculate the sigmoidal curves representing the time below (y-variate = min/d; ranging from 0 to 1440 min/d) each pH or temperature cutoff point (x-variate = pH or temperature values; ranging from 5.5 to 7.0 or from 35 to 41°C, respectively) by the logistic regression {y = a/[1 + e−(b + cx)]; with a being the maximum value and b and c being the regression coefficients} using the Solver Tool in Microsoft Excel (
      • Harris D.C.
      Nonlinear least-squares curve fitting with Microsoft Excel Solver.
      ), as indicated by
      • AlZahal O.
      • Kebreab E.
      • France J.
      • McBride B.W.
      Mathematical approach to predicting biological values from ruminal pH measurements.
      . This mathematical approach allowed the comparison of the inflection points, slopes and area under the curves (AUC) by integrating between 2 points (pH = 5.5 to 7.0; temperature = 35 to 41°C), making objective the interpretation of the rumen pH and temperature complexities throughout the day.
      Differences between least squares means were determined with the PDIFF option of SAS. Pearson correlations were used to determine the relationship between the studied variables. Significance was declared as P < 0.05, unless otherwise indicated.

      Results and Discussion

      Bolus sensors were found in the ventral sac of the goats at the surgery done at the end of each experiment. The overall pH sensor drift observed in both experiments was small and averaged 0.01 ± 0.02 and −0.02 ± 0.02, for pH 4.01 and 7.00, respectively. These results indicate the stability of the sensor measurements throughout the experiments, agreeing with the previous findings of
      • Mullins C.R.
      • Mamedova L.K.
      • Brouk M.J.
      • Moore C.E.
      • Green H.B.
      • Perfield K.L.
      • Smith J.F.
      • Harner J.P.
      • Bradford B.J.
      Effects of monensin on metabolic parameters, feeding behavior, and productivity of transition dairy cows.
      and
      • Hassanat F.
      • Gervais R.
      • Julien C.
      • Massé D.I.
      • Lettat A.
      • Chouinard P.Y.
      • Petit H.V.
      • Benchaar C.
      Replacing alfalfa silage with corn silage in dairy cow diets: Effects on enteric methane production, ruminal fermentation, digestion, N balance, and milk production.
      using the same type of bolus sensors in cows.

      Experiment 1

      Feed Intake and Water Consumption

      According to the imposed feeding conditions, no differences (P = 0.323) were detected in DMI or water consumption of the HF and LF goats (Table 2). Moreover, water intake was predicted from DMI by using the
      • Giger-Reverdin S.
      • Morand Fehr P.
      • Sauvant D.
      Water intake of dairy goats in intensive systems.
      equation for lactating dairy goats under temperate conditions. The measured value of water intake in our goats (3.64 ± 0.96 L/d, on average; Table 2) was 6% greater than the value estimated from the
      • Giger-Reverdin S.
      • Morand Fehr P.
      • Sauvant D.
      Water intake of dairy goats in intensive systems.
      equation (3.44 L/d). On average, our dry and open does drank 4.5 L/kg of DM of cold water, being able to consume the necessary amount of water under the restricted watering frequency conditions imposed in experiment 1 (i.e., once daily for 30 min). This ability of dairy goats to adapt to single watering is based on the use of the rumen as a water reservoir, as previously described by
      • Silanikove N.
      The physiological basis of adaptation in goats to harsh environments.
      .
      Table 2Feed and water intakes, rectal and rumen temperatures, rumen and urine pH in nonlactating dairy goats of experiment 1 fed diets containing 70 (HF; n = 8) or 30% forage (LF; n = 8); values are LSM
      ItemDietSED
      SED=standard error of the difference.
      Effect (P-value)
      HFLFTreatmentPeriodSequence
      Order of treatments.
      Daily intake
       DM, g866769770.3230.7830.378
       CP, g1049090.1700.8970.385
       NDF, g446263380.0050.9830.456
       ADF, g246126210.0030.9520.488
       NFC,
      Fermentable carbohydrates not recovered in NDF, referred to as nonfiber carbohydrates (OM − NDF − CP − fat).
      g
      296406420.0450.8560.567
       NEL, Mcal1.211.27
       Water, L3.543.750.960.7280.2280.878
      Rectal temperature, °C38.2238.160.130.6600.1610.464
      Rumen temperature, RT
       Average RT, °C38.8238.920.120.3960.1560.783
       RT ≥38.8, min/d9089381260.8510.6590.606
       RT ≥39.2, min/d5485401500.9680.6800.266
       RT ≥39.6, min/d3051201620.4580.6070.980
      Rumen pH6.566.250.060.0010.0480.001
      Urine pH7.657.670.200.9230.0630.540
      1 SED = standard error of the difference.
      2 Order of treatments.
      3 Fermentable carbohydrates not recovered in NDF, referred to as nonfiber carbohydrates (OM − NDF − CP − fat).

      Ruminal pH and Temperatures

      Mean daily rumen pH of HF goats was 0.31 units greater (P < 0.001) than that of LF goats (Table 2), according to their respective content in nonfiber carbohydrates as shown in Table 2. A similar effect on rumen pH was reported by
      • Cantalapiedra-Hijar G.
      • Yáñez-Ruiz D.R.
      • Martín-García A.I.
      • Molina-Alcaide E.
      Effects of forage:concentrate ratio and forage type on apparent digestibility, ruminal fermentation, and microbial growth in goats.
      in dry Granadina goats fed 70:30 or 30:70 forage-to-concentrate ratio diets (average pH 6.43 and 6.26, respectively); the diet with the highest proportion of concentrate produced more VFA and had a greater concentration of lactic acid in the rumen according to
      • Cantalapiedra-Hijar G.
      • Yáñez-Ruiz D.R.
      • Martín-García A.I.
      • Molina-Alcaide E.
      Effects of forage:concentrate ratio and forage type on apparent digestibility, ruminal fermentation, and microbial growth in goats.
      .
      Although we did not compare the rumen pH measured by the bolus sensors or by direct pH meters in the goats, the in vivo validation (done in our study using a rumen-cannulated dairy cow) showed agreement, albeit with medium correlation coefficients between both measures (rumen pH, r = 0.63; rumen temperature, r = 0.88; P < 0.001). Lower correlations were observed in cows (r = 0.59;
      • Lohölter M.
      • Rehage R.
      • Meyer U.
      • Lebzien P.
      • Rehage J.
      • Dänicke S.
      Evaluation of a device for continuous measurement of rumen pH and temperature considering localization of measurement and dietary concentrate proportion.
      ) and sheep (r = 0.46;
      • Kaur R.
      • Garcia S.C.
      • Horadagoda A.
      • Fulkerson W.J.
      Evaluation of rumen probe for continuous monitoring of rumen pH, temperature and pressure.
      fed diets with different forage-to-concentrate ratios, which may be a consequence of the differences between sampling points and type of sensors used.
      We are not aware of previous studies detailing rumen pH changes in goats over 24 h with short time intervals (i.e., every 30 min) as done in our does, but
      • Giger-Reverdin S.
      • Rigalma K.
      • Desnoyers M.
      • Sauvant D.
      • Duvaux-Ponter C.
      Effect of concentrate level on feeding behavior and rumen and blood parameters in dairy goats: Relationships between behavioral and physiological parameters and effect of between-animal variability.
      recently compared the effects of extreme forage-to-concentrate diets (70:30 and 40:60) in rumen-cannulated dairy goats at 2-h intervals during the first 8 h after feeding. On average, values of rumen pH and acetate-to-propionate ratio for the 70:30 versus 40:60 diets were 6.28 versus 5.96 and 3.62 versus 3.09, respectively, with rumen pH being permanently lower for the 40:60 diet according to
      • Giger-Reverdin S.
      • Rigalma K.
      • Desnoyers M.
      • Sauvant D.
      • Duvaux-Ponter C.
      Effect of concentrate level on feeding behavior and rumen and blood parameters in dairy goats: Relationships between behavioral and physiological parameters and effect of between-animal variability.
      . In our data, the values of the rumen pH differed according to diet (Figure 1), the pH of LF goats being lower than of HF goats for all time points (P < 0.01) except during the middle of the night from 9 to 14 h postfeeding (P = 0.124). Moreover, both goat groups did not differ on the initial and final rumen pH values (P = 0.325). For the HF goats, a decrease of 0.37 units in rumen pH was seen, with a descending phase until 12.5 h postfeeding at which the nadir (pH 6.35 ± 0.07) was observed. A further linear ascending phase until h 24 was observed (P < 0.001), as shown in Figure 1. Conversely, pH rapidly decreased in LF goats by 0.50 units during the first 6 h postfeeding, at which the nadir (pH 6.07 ± 0.07) was observed, increased from 6.5 to 9 h (P < 0.001), steadied from 9.5 to 18 h, and finally increased rapidly from 18 to 24 h (P < 0.001) to reach the initial value.
      Figure thumbnail gr1
      Figure 1Rumen pH (○ and ●) and rumen temperature (∆ and ▲) of nonlactating goats of experiment 1 fed diets with 70:30 (○, ∆; n = 8) or 30:70 (●, ▲; n = 8) forage-to-concentrate ratio at maintenance level. The solid arrow indicates the time of feed withdrawal and the open arrow indicates watering. The shaded area indicates natural night time (2000 to 0800 h). The SEM values were 0.03 and 0.13 for rumen pH and temperature, respectively.
      This change of curve pattern differs from that reported by
      • Giger-Reverdin S.
      • Rigalma K.
      • Desnoyers M.
      • Sauvant D.
      • Duvaux-Ponter C.
      Effect of concentrate level on feeding behavior and rumen and blood parameters in dairy goats: Relationships between behavioral and physiological parameters and effect of between-animal variability.
      , who observed a lower rumen pH before and at all time points after feeding in the goats fed the 40:60 diet, the rumen pH nadir occurring at 2 to 4 h after feeding and the goats showing signs of milk fat depression and evidence of SARA (i.e., lower blood pH, reduced intake, inverted fat-to-protein ratio in milk) when the rumen pH was under 6.0. This rumen pH threshold of 6.0 was not surpassed in our does.
      • Enemark J.M.D.
      • Peters G.
      • Jørgensen R.J.
      Continuous monitoring of rumen pH. A case study with cattle.
      and
      • Lohölter M.
      • Rehage R.
      • Meyer U.
      • Lebzien P.
      • Rehage J.
      • Dänicke S.
      Evaluation of a device for continuous measurement of rumen pH and temperature considering localization of measurement and dietary concentrate proportion.
      reported a fall in rumen pH after feeding in dairy cows fed high-forage or high-concentrate diets, the nadir occurring at 2 to 3 h postfeeding regardless of the diet. Moreover,
      • Lohölter M.
      • Rehage R.
      • Meyer U.
      • Lebzien P.
      • Rehage J.
      • Dänicke S.
      Evaluation of a device for continuous measurement of rumen pH and temperature considering localization of measurement and dietary concentrate proportion.
      reported that high-roughage diets induce a delayed microbial fermentation when compared with high-concentrate diets, which agrees with the slower reduction and later rumen pH nadir that was observed in our HF does, when compared with LF (Figure 1).
      The increases in rumen pH at 12 (HF goats) and 18 h (LF goats) postfeeding observed in our results may be a result of the buffering effect of the saliva entering the rumen during rumination (
      • Guilloteau P.
      • Le Huërou-Luron I.
      • Malbert C.H.
      • Toullec R.
      Les secretions digestives et leur regulation.
      ). At both times, the goats were without feed (i.e., removed 4 h postfeeding) and resting in the middle of the night. The greater fiber content and particle size in the HF diet, when compared with the LF diet, may have produced a longer rumination time and a greater buffering effect of the saliva in the rumen of the HF goats.
      Rumen pH was modeled according to
      • AlZahal O.
      • Kebreab E.
      • France J.
      • McBride B.W.
      Mathematical approach to predicting biological values from ruminal pH measurements.
      by accounting for the amount of time spent below pH cut-off points for both diets (Figure 2a). The values of the inflection points (y = 720 min/d) on the sigmoidal curves for the HF (pH = 6.50) and LF (pH = 6.25) diets, representative of the ruminal acid-base neutralization reaction kinetics, were close to the average pH values reported in Table 2. Moreover, the AUC between pH 5.5 and 7.0 were 718 ± 145 and 1,083 ± 224 min/d for HF and LF, respectively (P = 0.038). Despite the difference in forage-to-concentrate ratio between diets, the slopes of the sigmoidal curves were similar between HF and LF diets (P > 0.05), indicating a similar buffering capacity of the rumen of both groups of goats.
      Figure thumbnail gr2
      Figure 2Logistic regression models for (a) the average rumen pH of goats of experiment 1 fed diets with 70:30 (– – –; y=14401+e57.8968.903x; R2 = 0.986) or 30:70 (——; y=14401+e61.6529.867x; R2 = 0.976) forage-to-concentrate ratio at maintenance level; and (b) the average rumen temperature of goats fed diets with 70:30 (– – –; y=14401+e96.4662.477x; R2 = 0.989) or 30:70 (——; y=14401+e108.5372.787x; R2 = 0.991) forage-to-concentrate ratio at maintenance level. All regressions were P < 0.001. The y-axis represents the accumulated time (min/d) spent below each corresponding pH or temperature (°C) point on the x-axis.
      Rumen temperature values averaged 38.9 ± 0.1°C and no differences were detected by diet throughout the experiment (P = 0.396; Table 2), which may be a consequence of feeding at maintenance level.
      • AlZahal O.
      • Steele M.A.
      • Valdes E.V.
      • McBride B.W.
      Technical note: The use of a telemetric system to continuously monitor ruminal temperature and to predict ruminal pH in cattle.
      ,
      • AlZahal O.
      • AlZahal H.
      • Steele M.A.
      • Van Schaik M.
      • Kyriazakis I.
      • Duffield T.F.
      • McBride B.W.
      The use of a radiotelemetric ruminal bolus to detect body temperature changes in lactating dairy cattle.
      ),
      • Wahrmund J.L.
      • Ronchesel J.R.
      • Krehbiel C.R.
      • Goad C.L.
      • Trost S.M.
      • Richard C.J.
      Ruminal acidosis challenge impact on ruminal temperature in feedlot cattle.
      , and
      • Lohölter M.
      • Rehage R.
      • Meyer U.
      • Lebzien P.
      • Rehage J.
      • Dänicke S.
      Evaluation of a device for continuous measurement of rumen pH and temperature considering localization of measurement and dietary concentrate proportion.
      reported greater rumen temperature with high-concentrate (40 to 65%) diets in cattle fed ad libitum. Heat is a by-product of microbial fermentation (
      • Hungate R.E.
      ) and, therefore, diets containing a greater proportion of concentrate (i.e., greater fermentable OM) should generate a faster and greater peak of heat within the rumen when compared with high-forage diets (
      • Arieli A.
      • Aharoni Y.
      • Zamwel S.
      • Tagari H.
      Effect of ratio of roughage concentrate on glucose-induced heat production in sheep rumen fluid in vitro.
      ;
      • Lohölter M.
      • Rehage R.
      • Meyer U.
      • Lebzien P.
      • Rehage J.
      • Dänicke S.
      Evaluation of a device for continuous measurement of rumen pH and temperature considering localization of measurement and dietary concentrate proportion.
      ). Rumen temperature increased (P < 0.001) by 0.82 and 1.25°C at 30 and 60 min postfeeding, respectively, due to the increase in rumen fermentation activity in both goat groups, and remained elevated until drinking. Conversely, rumen temperature decreased by 3.42 and 3.51°C (P < 0.001) at 30 and 60 min after drinking in HF and LF does, respectively (Figure 1). Afterward, values of rumen temperature recovered and gradually increased, but never reached the predrinking values because most feed was already consumed. During the last 3.5 h before the following meal, rumen temperatures slowly decreased and were similar (P = 0.135 to 0.812) to those before feeding (Figure 1).
      Values of rumen temperature were also modeled using the logistic regression for both diets (Figure 2b). Despite the forage-to-concentrate ratio values used in the HF and LF diets, the inflection points (y = 720 min/d), representative of heat production kinetics in the rumen, mean temperature values (38.96 ± 0.15 and 38.95 ± 0.12°C; P = 0.876), and AUC between 35 and 41°C (2,963 ± 345 and 2,962 ± 478 min/d and °C; P = 0.987) were similar and close to the average temperatures reported in Table 2 for the HF and LF diets, respectively.
      Does in the current experiment drank on average 3.9 ± 0.7 L (10% of BW) of cold water (9.8 ± 0.4°C) within 5 to 10 min. The decrease in rumen temperature after drinking in the current study (−3.4°C at 30 min) was much lower than that reported by
      • Bewley J.M.
      • Grott M.W.
      • Einstein M.E.
      • Schutz M.M.
      Impact of intake water temperatures on reticular temperatures of lactating dairy cows.
      in dairy cows (−8.5°C at 15 min) drenched with 25 L (4% BW approximately) of cold water (7.6°C). In the later study, rumen temperature recovered at 3.5 h after water drenching, but in our results the values returned to normal range within 2 h. It should be taken into account that boluses in the study of
      • Bewley J.M.
      • Grott M.W.
      • Einstein M.E.
      • Schutz M.M.
      Impact of intake water temperatures on reticular temperatures of lactating dairy cows.
      were located in the reticulum, whereas in our goats boluses were in the ventral sac, which might explain differences in the magnitude of temperature reduction after drinking. We detected a positive correlation (r = 0.59; P < 0.05) between the amount of water consumed (2.6 to 5.8 L) and the decrease in rumen temperature (−2.4 to −5.6°C) 30 min after water consumption. Drinking cold water may have produced a decrease in the body temperature of the goats, as reported by
      • Bewley J.M.
      • Grott M.W.
      • Einstein M.E.
      • Schutz M.M.
      Impact of intake water temperatures on reticular temperatures of lactating dairy cows.
      in cows, and could be recommended as a strategy for alleviating HS during the hot hours of the day in lactating ruminants.
      Because rumen temperature increased and rumen pH decreased after feeding, a negative low correlation was observed (r = −0.33; P < 0.05) between both variables in our study, which agrees with the reports of
      • Wahrmund J.L.
      • Ronchesel J.R.
      • Krehbiel C.R.
      • Goad C.L.
      • Trost S.M.
      • Richard C.J.
      Ruminal acidosis challenge impact on ruminal temperature in feedlot cattle.
      ; r = −0.64 to 0.09) and
      • Lohölter M.
      • Rehage R.
      • Meyer U.
      • Lebzien P.
      • Rehage J.
      • Dänicke S.
      Evaluation of a device for continuous measurement of rumen pH and temperature considering localization of measurement and dietary concentrate proportion.
      ; r = −0.11) using rumen sensors in steers and cows, respectively. This inverse relationship can be used to predict the rumen pH when related to critical points, as indicated by
      • AlZahal O.
      • Kebreab E.
      • France J.
      • Froetschel M.
      • McBride B.W.
      Ruminal temperature may aid in the detection of subacute ruminal acidosis.
      , who reported R2 = 0.77 between minimum rumen pH and its corresponding rumen temperature in cows. Correlation between minimum rumen pH and corresponding rumen temperature was R2 = 0.64 (P < 0.001) in our data.

      Rectal Temperature and Relationship with Ruminal Temperature

      No effect of the diet on rectal temperatures were detected (Table 2), agreeing with the findings of
      • AlZahal O.
      • AlZahal H.
      • Steele M.A.
      • Van Schaik M.
      • Kyriazakis I.
      • Duffield T.F.
      • McBride B.W.
      The use of a radiotelemetric ruminal bolus to detect body temperature changes in lactating dairy cattle.
      in cows. Conversely, rectal temperatures increased throughout the day (0900 h = 37.5 ± 0.2°C; 1300 h = 38.4 ± 0.2°C; 1700 h = 38.8 ± 0.2°C; P = 0.008) by an effect of the rumen fermentation heat and the increase of ambient temperatures (from 10 to 16°C).
      Rumen temperatures were, on average, 0.68 ± 0.06°C greater than rectal temperatures, agreeing with
      • AlZahal O.
      • AlZahal H.
      • Steele M.A.
      • Van Schaik M.
      • Kyriazakis I.
      • Duffield T.F.
      • McBride B.W.
      The use of a radiotelemetric ruminal bolus to detect body temperature changes in lactating dairy cattle.
      , and increased throughout the day (0900 h = 38.2 ± 0.2°C; 1300 h = 39.5 ± 0.2°C; 1700 h = 39.6 ± 0.2°C; P < 0.001). A high and positive correlation was detected between both rectal and rumen temperatures (r = 0.91; P < 0.001).

      Experiment 2

      Feed Intake

      Decrease of DMI due to HS usually ranges between 20 and 35% in lactating dairy goats fed ad libitum and according to stage of lactation (
      • Hamzaoui S.
      • Salama A.A.K.
      • Caja G.
      • Albanell E.
      • Flores C.
      • Such X.
      Milk production losses in early lactating dairy goats under heat stress.
      ,
      • Hamzaoui S.
      • Salama A.A.K.
      • Albanell E.
      • Such X.
      • Caja G.
      Physiological responses and lactational performances of late lactating dairy goats under heat stress conditions.
      ). In our data, HS goats reduced their intake by 13%, although the difference between TN and HS treatments was not significant (Table 3; P = 0.18). It should be stressed that they were nonlactating and fed at maintenance level and, despite not differing in DMI, the TN goats gained and the HS goats lost BW during the experiment (Table 3), indicating a negative energy balance in the HS goats. Greater energy maintenance requirements during HS are expected to cover the needs for extra activities related to physical activity (i.e., panting), greater sweating, increased chemical reactions in the body, and the production of HS proteins that consume large amounts of ATP (
      • McDowell R.E.
      • Moody E.G.
      • Van Soest P.J.
      • Lehmann R.P.
      • Ford G.L.
      Effect of heat stress on energy and water utilization of lactating cows.
      ;
      • Beede D.K.
      • Collier R.J.
      Potential nutritional strategies for intensively managed cattle during thermal stress.
      ;
      • Salama A.A.K.
      • Caja G.
      • Hamzaoui S.
      • Badaoui B.
      • Castro-Costa A.
      • Façanha D.A.E.
      • Guilhermino M.M.
      • Bozzi R.
      Different levels of response to heat stress in dairy goats.
      ).
      Table 3Body weight, DM and water intakes, respiration rate, rectal and rumen temperatures, and rumen pH of nonlactating goats of experiment 2 under thermal neutral (TN, n = 8) or heat stress (HS, n = 8) conditions; values are LSM
      ItemTreatmentSED
      SED=standard error of the difference.
      Effect (P-value)
      TNHSTreatmentPeriodSequence
      Order of treatments.
      Initial BW, kg43.144.71.60.2670.2410.120
      Final BW, kg44.443.31.40.4690.2870.080
      BW change, kg1.3−1.41.10.0330.0130.633
      DMI, kg/d1.130.980.100.1830.9440.971
      Water consumption, L/d2.25.40.70.0020.2380.960
      Respiration rate, breaths/min2810550.0010.3220.428
      Rectal temperature, °C38.639.00.10.0010.2760.134
      Rumen temperature, °C39.639.90.10.0040.4450.721
      Rumen pH6.556.430.040.0030.0010.450
      Urine pH7.797.770.090.8340.3350.265
      1 SED = standard error of the difference.
      2 Order of treatments.

      Ruminal pH and Temperature

      On average, rumen pH of TN and HS goats decreased by 0.51 ± 0.05 units at 3 h postfeeding, reaching the rumen pH nadir at a similar time. Despite eating the same diet and a similar DMI, mean daily rumen pH of the HS goats was 0.12 units lower than that of TN goats (Table 3; P < 0.01). At most postfeeding time points, rumen pH of HS goats was lower than TN goats, although the difference was only significant for the interval 12 to 18 h after feeding (on average, −0.21 ± 0.05 units; P < 0.001). This time interval occurred during the night (shaded area in Figure 3) when the goats had finished their diet and were expected to be resting and ruminating. We hypothesized that HS goats had shorter rumination time as a consequence of panting, which produced a lower saliva secretion and impaired rumen buffering capacity, resulting in a lower rumen pH. Similar to our results,
      • Mishra M.
      • Martz F.A.
      • Stanley R.W.
      • Johnson H.D.
      • Campbell J.R.
      • Hilderbrand E.
      Effect of diet and ambient temperature-humidity on ruminal pH, oxidation reduction potential, ammonia and lactic acid in lactating cows.
      and
      • Bandaranayaka D.D.
      • Holmes C.W.
      Changes in the composition of milk and rumen contents in cows exposed to a high ambient temperature with controlled feeding.
      reported that rumen pH in HS cows was lower than in TN cows fed a similar amount of DM.
      Figure thumbnail gr3
      Figure 3Ruminal pH (○ and ●) and ruminal temperature (∆ and ▲) of goats of experiment 2 under thermal neutral (○, ∆; n = 8) or heat stress (●, ▲; n = 8) conditions. The shaded area indicates artificial night time (2100 to 0900 h) during which ambient temperature was reduced from 37 to 30°C for heat-stressed goats. Outside this time interval, heat-stressed goats were exposed to 37°C. The SEM values were 0.05 and 0.14 for rumen pH and temperature, respectively.
      Logistic models of rumen pH values for TN and HS diets are shown in Figure 4a. The inflection points on the sigmoidal curves (y = 720 min/d) for both TN (pH = 6.53) and HS (pH = 6.40) were different according to conditions and close to the average pH values reported in Table 3, the AUC from pH 5.5 to 7.0 being lower for TN than HS does (675 ± 128 vs. 862 ± 165 min/d and pH unit, respectively; P = 0.046).
      Figure thumbnail gr4
      Figure 4Logistic regression models for (a) the average rumen pH of goats of experiment 2 under thermoneutral (– – –; y=14401+e66.45710.174x; R2 = 0.974) or heat stress (——; y=14401+e57.4508.974x; R2 = 0.987) conditions; and (b) the average rumen temperature of goats under thermoneutral (– – –; y=14401+e316.4057.987x; R2 = 0.952) or heat stress (——; y=14401+e277.8306.965x; R2 = 0.963) conditions and fed a diet with 50:50 forage-to-concentrate ratio at maintenance level. All regressions were P < 0.001. The y-axis represents the accumulated time (min/d) spent below each corresponding pH or temperature (°C) point on the x-axis.
      Rumen temperature evolution pattern was the opposite of that observed for rumen pH (Figure 3), increasing after feeding and slowly decreasing during the nocturnal period. The HS goats showed greater rumen temperature (0.3 ± 0.1°C; P = 0.004) than TN goats before feeding (Table 3) in accordance with the high ambient temperature under which the HS does were kept. Rectal temperature values were also greater (by 0.4 ± 0.1°C; P = 0.001) in the HS does, agreeing with the previously indicated rumen and ambient temperatures effects. As far as we know, rumen temperature has not been evaluated in farm animals under TN and HS conditions. Compared with values before feeding, TN and HS rumen temperatures increased at 1.5 h postfeeding (0.23°C; P < 0.01) and peaked at 8 h postfeeding (0.52°C; P < 0.001), gradually decreasing thereafter with the difference not being significant (P = 0.467) after 16.5 h postfeeding. There was no interaction treatment × hour (P = 0.721) for rumen temperature.
      Rumen temperature values were also modeled using the logistic regression (Figure 4b), showing inflection points (y = 720 min/d) at 39.62 and 39.89°C for the TN and HS conditions, which were close to the average temperature values reported in Table 3. Moreover the AUC from 35 to 41°C also differed according to the environmental conditions (TN = 1,994 ± 276 min/d and °C; HS = 1,599 ± 198 min/d and °C; P = 0.008).
      Rumen temperature and pH correlated in the whole goat data (y = −0.457x + 24.63; r = −0.73; root mean square error = 0.19; P < 0.01), but not enough related to be used for prediction purposes. Rumen and rectal temperatures also showed a positive relationship (R2 = 0.62; P < 0.01), the rumen temperature being greater than the rectal temperature (0.95 ± 0.11°C, on average) in our dry and open goats, greater than the value obtained in experiment 1 under different feeding conditions.

      Water Intake

      As water was freely available at ambient temperature (i.e., 20 to 23°C for TN, 30 to 37°C for HS), no marked decrease in rumen temperature was observed after drinking (Figure 3) such as those which occurred in experiment 1 when goats drank cold water once daily. Effects of HS in the rumen temperature of our goats were not mitigated by drinking cold water, as reported by
      • Bewley J.M.
      • Grott M.W.
      • Einstein M.E.
      • Schutz M.M.
      Impact of intake water temperatures on reticular temperatures of lactating dairy cows.
      in dairy cows. Although we did not observe drops in the rumen temperature of the goats during the whole day, small drops hardly detectable were observed in rumen temperatures at 3 and 4 h after feeding (Figure 3) in the TN and HS goats, most likely as a result of drinking water at ambient temperature.

      Digestibility Coefficients

      Digestibility coefficients did not vary between TN and HS goats (Table 4). Previous results observed by
      • Hamzaoui S.
      • Salama A.A.K.
      • Albanell E.
      • Such X.
      • Caja G.
      Physiological responses and lactational performances of late lactating dairy goats under heat stress conditions.
      ,
      • Hamzaoui S.
      • Salama A.A.K.
      • Caja G.
      • Albanell E.
      • Such X.
      Supplementation with soybean oil increases milk fat and improves milk fatty acid profile in heat-stressed dairy goats.
      ) in lactating goats of the same breed fed ad libitum, showed improvements (3 to 9 points) in the digestibility coefficients of DM, CP, NDF, and ADF by the effect of HS. Moreover, HS increased the diet digestibility in male goats (
      • Hirayama T.
      • Katoh K.
      • Obara Y.
      Effects of heat exposure on nutrient digestibility, rumen contraction and hormone secretion of goats.
      ), dairy cows (
      • McDowell R.E.
      • Moody E.G.
      • Van Soest P.J.
      • Lehmann R.P.
      • Ford G.L.
      Effect of heat stress on energy and water utilization of lactating cows.
      ), and dairy heifers (
      • Bernabucci U.
      • Bani P.
      • Ronchi B.
      • Lacetera N.
      • Nardone A.
      Influence of short- and long-term exposure to a hot environment on rumen passage rate and diet digestibility by Friesian heifers.
      ). In all mentioned studies, DMI decreased by HS, which might explain the increment of digestibility as a consequence of the depressed passage rate of the solid phase of digesta throughout the gastrointestinal tract, as reported by
      • Silanikove N.
      • Tagari H.
      • Shkolnik A.
      Comparison of rate of passage, fermentation rate and efficiency of digestion of high fiber diet in desert Bedouin goats compared to Swiss Saanen goats.
      and
      • Bernabucci U.
      • Bani P.
      • Ronchi B.
      • Lacetera N.
      • Nardone A.
      Influence of short- and long-term exposure to a hot environment on rumen passage rate and diet digestibility by Friesian heifers.
      . In the current study, DMI was similar between groups and, consequently, differences in digestibilities were minimal.
      Table 4Digestibility coefficients of nonlactating goats of experiment 2 under thermal neutral (TN, n = 8) or heat stress (HS, n = 8) conditions; values are LSM
      ItemTreatmentSED
      SED=standard error of the difference.
      Effect (P-value)
      TNHSTreatmentPeriodSequence
      Order of treatments.
      DM75.877.72.20.4210.3260.373
      OM78.379.82.10.5130.3590.425
      CP77.479.12.00.4230.1830.178
      NDF51.156.64.20.2300.2790.737
      ADF50.152.64.80.2110.1640.875
      1 SED = standard error of the difference.
      2 Order of treatments.

      Blood Measures

      Although HS goats lost BW, they were able to maintain a similar blood glucose and urea concentrations to TN goats (Table 5) in the short term, which agreed with their similar intake (Table 3) and nutrient digestibilities (Table 4) observed under our feeding conditions and agrees with
      • Hamzaoui S.
      • Salama A.A.K.
      • Albanell E.
      • Such X.
      • Caja G.
      Physiological responses and lactational performances of late lactating dairy goats under heat stress conditions.
      and
      • Sano H.
      • Ambo K.
      • Tsuda T.
      Blood glucose kinetics in whole body and mammary gland of lactating goats exposed to heat stress.
      in dairy goats and dairy ewes, respectively. Moreover, HS goats have been shown to have a pancreas less responsive in insulin secretion to a glucose tolerance test than TN goats as well as having kidneys that are able to produce glucose (
      • Salama A.A.K.
      • Caja G.
      • Hamzaoui S.
      • Badaoui B.
      • Castro-Costa A.
      • Façanha D.A.E.
      • Guilhermino M.M.
      • Bozzi R.
      Different levels of response to heat stress in dairy goats.
      ), these mechanisms allowing them to maintain the values of blood glucose during HS.
      Table 5Metabolic and acid-base balance indicators of nonlactating goats of experiment 2 under thermal neutral (TN, n = 4) or heat stress (HS, n = 4) conditions; values are least squares means
      ItemTreatmentSED
      SED=standard error of the difference.
      Effect

      (P-value)
      TNHS
      Glucose, mg/dL57.755.05.20.630
      Urea, mg/dL14.313.31.80.571
      Na, mmol/L14915210.021
      K, mmol/L3.473.830.300.292
      Cl, mmol/L11111920.017
      Hematocrit, %PCV
      PCV=packed cell volume.
      18.315.31.00.032
      Hemoglobin,
      Calculated by the VetScan i-STAT 1 device software (Abaxis, Union City, CA).
      mmol/L
      6.235.180.370.034
      pH7.457.470.020.510
      Total CO2,
      Calculated by the VetScan i-STAT 1 device software (Abaxis, Union City, CA).
      mmol/L
      302220.009
      Anion gap,
      Calculated by the VetScan i-STAT 1 device software (Abaxis, Union City, CA).
      mmol/L
      12.715.51.10.044
      CO2 pressure, mmHg422930.006
      HCO3,
      Calculated by the VetScan i-STAT 1 device software (Abaxis, Union City, CA).
      mmol/L
      28.821.11.80.007
      Base excess
      Calculated by the VetScan i-STAT 1 device software (Abaxis, Union City, CA).
      4.67−2.751.970.010
      1 SED = standard error of the difference.
      2 PCV = packed cell volume.
      3 Calculated by the VetScan i-STAT 1 device software (Abaxis, Union City, CA).
      Blood pH was similar between TN and HS goats (Table 5), despite the increase in respiration rate reported in Table 3. An accelerated respiration rate (panting) is an important thermoregulatory response to HS and a key way for heat dissipation through evaporative cooling (
      • Blackshaw J.K.
      • Blackshaw A.W.
      Heat stress in cattle and the effect of shade on production and behaviour: A review.
      ;
      • Silanikove N.
      The struggle to maintain hydration and osmoregulation in animals experiencing severe dehydration and rapid rehydration: the story of ruminants.
      ;
      • Beatty D.T.
      • Barnes A.
      • Taylor E.
      • Pethick D.
      • McCarthy M.
      • Maloney S.K.
      Physiological responses of Bos taurus and Bos indicus cattle to prolonged, continuous heat and humidity.
      ). Panting eliminates pulmonary CO2 faster than it is produced and, consequently, reduces blood CO2 pressure, which tends to raise blood pH and decrease the concentration of HCO3 and its buffer role. To restore the pH to normal, panting must be stopped or the kidneys must eliminate HCO3. The latter occurs because the low blood CO2 pressure and alkalosis reduce H+ and NH3 production by the kidneys (
      • Calamari L.
      • Abeni F.
      • Calegari F.
      • Stefanini L.
      Metabolic conditions of lactating Friesian dairy cows during the hot season in the Po valley. 2. Blood minerals and acid-base chemistry.
      ).
      In our data, increased alveolar ventilation contributed to a greater pulmonary loss of CO2 and to a decrease in blood CO2 pressure and total CO2 of HS goats (P < 0.01; Table 5), decreasing HCO3 and base excess in the blood of HS goats to maintain constant blood pH (P < 0.01; Table 5). No effects were detected on urea in plasma (P = 0.570). The reduction in blood HCO3 concentration under HS leads to a decrease in the buffering capacity of the saliva arriving to the rumen (
      • Guilloteau P.
      • Le Huërou-Luron I.
      • Malbert C.H.
      • Toullec R.
      Les secretions digestives et leur regulation.
      ) and, consequently, lower rumen pH, as observed in our HS goats.
      Hematocrit and hemoglobin values were lower (P = 0.034) in HS than TN goats (Table 5).
      • Weldy J.R.
      • McDowell R.E.
      • Van Soest P.J.
      • Bond J.
      Influence of heat stress on rumen acid levels and some blood constituents in cattle.
      reported a negative correlation (r = −0.44) between blood cell volume and rectal temperature under HS conditions in dairy cows. It seems that increased water consumption by HS does (Table 3) caused an hemodilution effect by increasing the plasma volume, the extra water amount being incorporated into the circulatory system for evaporative cooling (
      • Silanikove N.
      Effects of water scarcity and hot environment on appetite and digestion in ruminants: A review.
      ).

      Conclusions

      Ruminal pH and temperature sensors were able to record a large amount of data (>10,000) that was useful to detect diurnal fluctuations of ruminal pH and temperature in relation to management and environmental changes. Continuous recording allowed modeling and measuring the amount of time spent below a critical pH or temperature points, which could add further soundness to the interpretation of data. By means of these sensors, we were able to detect a lower rumen pH in HS goats, even when they had similar feed intake to goats under TN conditions. Effects of water temperature and changes in rumen fermentation and absorption of metabolites across the rumen wall under same nutrition and HS conditions need further research.

      Acknowledgments

      This work is part of a research project (Plan Nacional I+D+I, Project AGL-2013-44061R) funded by the Spanish Ministry of Economy and Finances (Madrid, Spain). The authors are also grateful to Ramon Costa and the team of the Servei de Granges i Camps Experimentals of the Universitat Autònoma de Barcelona (Bellaterra, Barcelona, Spain) for the care of the animals, to Kahne Ltd. (Auckland, New Zealand) for the technical support, and to Nic Aldam (Barcelona, Spain) for the English revision of the manuscript.

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