Coprophagous behavior of rabbit pups affects implantation of cecal microbiota and health status

During the first few weeks after delivery, female rabbits excrete fecal pellets, which are ingested by their pups. We hypothesized that maternal excretion of hard fecal pellets and the coprophagous behavior of their pups were involved in cecal microbiota implantation. Four groups were compared: in 1 group (FM), pups had free access to maternal fecal pellets; in a second group, ingestion of feces was prevented (NF); and in 2 additional groups, pups had access only to fecal pellets excreted by foreign females receiving either no antibiotic (FF) or tiamulin and tetracycline (FFab). A total of 109 litters in 3 batches were used to quantify excretion and ingestion of feces and mortality. Bacterial composition was assessed by 454 pyrosequencing of the V3 to V4 region of 16S RNA genes and fermentative measurements in 128 rabbits of 1 batch at age 14, 35, 49, and 80 d with 8 rabbits per group for each age with 2 rabbits per litter. The number of fecal pellets excreted by does from 2 to 20 d after delivery ranged widely, but was similar among groups (16.1 +/- 12.6 fecal pellets/doe). The excretion peaked during the first 6 d after delivery. Foreign fecal ingestion (FF and FFab groups) was 3 times greater (P < 0.001) than ingestion of maternal feces (9.9 +/- 7.8). Ingestion of feces in the FF group was greater than in the FFab groups (35.6 +/- 9.3 vs. 29.5 +/- 9.7; P < 0.05). Compared with the FM group, ingestion of feces in the FF and FFab groups began later (6 to 7 d vs. 2 to 3 d after birth) and peaked at 14 to 17 d (4.0 +/- 1.8 hard fecal pellets.litter(-1).d(-1)) and 13 to 15 d (3.5 +/- 1.7 hard fecal pellets litter(-1) d(-1)), respectively. During the 36 to 49 d period, the FF and NF groups exhibited the least (2.8%) and greatest (9.5%) mortality, respectively (P = 0.03). At age 14 d, the cecal bacterial community was dominated by Bacteroidetes phyla (63.3 +/- 15.1%), Bacteroidaceae family (36.0 +/- 18.8%), and Bacteriodes genus (36.0 +/- 2.3%). With increasing age, Firmicutes phyla, Lachnospiraceae, and Ruminococcaceae families became the dominant taxa (92.0 +/- 4.7, 44.0 +/- 13.7, 37.9 +/- 11.6% at age 80 d, respectively). Impairment of fecal ingestion delayed this ecological succession, with greater and lower relative abundance of Bacteroidaceae and Ruminococcaceae, respectively, than in the other 3 groups at age 35 d (P < 0.10). In conclusion, although excretion of hard fecal pellets by does ranged widely, the coprophagous behavior of their pups affected the implantation of cecal bacterial microbiota.