Phenological changes in bamboo carbohydrates explain the preference for culm over leaves by giant pandas (Ailuropoda melanoleuca) during spring

Abstract

Seasonal changes in the foodscape force herbivores to select different plant species or plant parts to meet nutritional requirements. We examined whether the search for calorie-rich carbohydrates explained giant panda’s selection for bamboo culm over leaves during spring. Leaves and culms were collected from four Phyllostachys bamboos (P. aurea, P. aureosulcata, P. glauca, and P. nuda) once per month over 18–27 months. Monthly changes in annual plant part nutrients were examined, and compared to seasonal foraging behaviors of captive giant pandas. Although total fiber was greater (p<0.0001) in culm (85.6 ± 0.5%) than leaves (55.3 ± 0.4%) throughout the year, culm fiber was at its lowest in spring (79–85%) when culm selection by giant pandas exceeded 70% of their overall diet. Culm starch also was greatest (p = 0.044) during spring (5.5 ± 1.1%) and 2.5-fold the percentage of starch in leaves (2.2 ± 0.6%). The free sugars in spring culm consisted of a high proportion of glucose (35%) and fructose (47%), whereas sucrose made up 42% of the total free sugar content of spring leaves. Bound sugars in culm consisted of 60% glucose and 38% xylose likely representative of hemicellulose. The concentrations of bound sugars (hemicelluloses) in spring culms (543.7 ± 13.0 mg/g) was greater (p<0.001) than in leaves (373.0 ± 14.8 mg/g). These data help explain a long-standing question in giant panda foraging ecology: why consume the plant part with the lowest protein and fat during the energetically intensive spring breeding season? Giant pandas likely prefer spring culm that contains abundant mono- and polysaccharides made more bioavailable as a result of reduced fiber content. These data suggest that phenological changes in bamboo plant part nutrition drive foraging decisions by giant pandas.

Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to Lactate

“…Pandas are extremely selective upon choosing which bamboo component to eat (i.e., shoots, leaves, branches, or stem) (Dierenfeld et al, 1982;Mainka et al, 1989;Edwards et al, 2006). Leaves are generally consumed all year long, however, a typical peak in stems consumption between March and May has been observed (Hansen et al, 2010;Williams et al, 2013;Knott et al, 2017) in both captive and wild pandas (Schaller et al, 1985;Taylor and Zisheng, 1987;Rybiski Tarou et al, 2005). As bamboo is an evergreen plant with leaves available throughout the year, the exact biological mechanisms motivating a dietary shift to stems remains unexplained.…”

“…Removal of the waxy outer cover from culms to get access to the softer, yellow pith before ingestion is a common behavior also in the wild (Schaller et al, 1985), and possibly linked to bamboo composition. A present assumption considers seasonal variation in bamboo nutrient content a reason for pandas' dietary behavior (Knott et al, 2017). However, it appears counterproductive to forage on the less digestible, woody pith during the panda's breeding season (March to April), when extra energy is spent to seek mates (Wildt et al, 2006).…”

“…Although not representative of the entire gastrointestinal tract, gut microbiomes in giant pandas are generally inferred using microbial communities from stool samples. Such microbial communities have been investigated for their assemblage (Zhu et al, 2011), how they related to dietary shifts (Sims et al, 2007;Williams et al, 2013;Knott et al, 2017) and for their potential cellulose (Zhu et al, 2011), hemicellulose (Zhang et al, 2018) or lignin biodegradation capacity (Fang et al, 2012), as assessed by metagenome analysis. However, no attempt was made so far to cultivate gut microbiomes to mimic giant panda's feeding.…”

Prospective Study on the Excretion of Mucous Stools and its Association with Age, Gender, and Feces Output in Captive Giant Pandas

“…The mucus occurrence peak in October might possibly be related to the diet transition from culm to leaves due to the feeding preferences of the pandas in this study, which may cause an increased occurrence of mucus excretion [4,5]. In addition, a feeding behavior study showed that the leaf was the primary plant part consumed from June to December, whereas culm was consumed primarily from February to May [24]. Another nutrition experiment showed that the total fiber was always greater in the culm than in the leaves throughout the year [25].…”

Dietary protein supplementation and its consequences for intake, digestion, and physical activity of a carnivorous marsupial, Sminthopsis crassicaudata

“…There is wide variation in the availability and nutritional composition of foods in nature, and thus animals are often faced with deficient or imbalanced diets. As a consequence, many animals have evolved diet regulation behaviors to maintain a balanced nutrient intake (Knott et al., ; Simpson, Sibly, Lee, Behmer, & Raubenheimer, ). Yet, in some cases, restricted diet choices or food availability may limit the ability of animals to regulate their macronutrient intake to their desired or target levels (Moore, Wiggins, Marsh, Dearing, & Foley, ; Simpson et al., ).…”