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Digestive Enzyme Activities and Gastrointestinal Fermentation in Wood-Eating Catfishes

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Digestive Enzyme Activities and Gastrointestinal Fermentation in Wood-Eating Catfishes UC Irvine UC Irvine Previously Published Works Title Digestive enzyme activities and gastrointestinal fermentation in wood-eating catfishes Permalink https://escholarship.org/uc/item/1p88v3g4 Journal Journal of Comparative Physiology B: Biochemical, Systems, and Environmental Physiology, 179(8) ISSN 1432-136X Authors German, Donovan P. Bittong, Rosalie A. Publication Date 2009-11-01 DOI 10.1007/s00360-009-0383-z Peer reviewed eScholarship.org Powered by the California Digital Library University of California J Comp Physiol B (2009) 179:1025–1042 DOI 10.1007/s00360-009-0383-z ORIGINAL PAPER Digestive enzyme activities and gastrointestinal fermentation in wood-eating catWshes Donovan P. German · Rosalie A. Bittong Received: 27 March 2009 / Revised: 11 June 2009 / Accepted: 16 June 2009 / Published online: 1 July 2009 © The Author(s) 2009. This article is published with open access at Springerlink.com Abstract To determine what capabilities wood-eating and -glucosidase and N-acetyl--D-glucosaminidase enzymes W W detritivorous cat shes have for the digestion of refractory were signi cantly lower than the Km values of microbial polysaccharides with the aid of an endosymbiotic microbial enzymes ingested with their food, further suggesting that the community, the pH, redox potentials, concentrations of Wsh eYciently digest soluble components of their detrital diet short-chain fatty acids (SCFAs), and the activity levels of 14 rather than refractory polysaccharides. Coupled with rapid digestive enzymes were measured along the gastrointestinal gut transit and poor cellulose digestibility, the wood-eating (GI) tracts of three wood-eating taxa (Panaque cf. nigroline- catWshes appear to be detritivores reliant on endogenous atus “Marañon”, Panaque nocturnus, and Hypostomus pyrin- digestive mechanisms, as are other loricariid catWshes. This eusi) and one detritivorous species (Pterygoplichthys stands in contrast to truly “xylivorous” taxa (e.g., beavers, disjunctivus) from the family Loricariidae. Negative redox termites), which are reliant on an endosymbiotic community potentials (¡600 mV) were observed in the intestinal Xuids of microorganisms to digest refractory polysaccharides. of the Wsh, suggesting that fermentative digestion was possi- ble. However, SCFA concentrations were low (<3 mM in Keywords Digestive enzymes · Xylivory · Fermentation any intestinal region), indicating that little GI fermentation occurs in the Wshes’ GI tracts. Cellulase and xylanase activi- ties were low (<0.03 U g¡1), and generally decreased distally Introduction in the intestine, whereas amylolytic and laminarinase activi- ties were Wve and two orders of magnitude greater, respec- The consumption of wood for food is rare among animals. tively, than cellulase and xylanase activities, suggesting that Unlike the “greener” portions of plants, woody tissues are the Wsh more readily digest soluble polysaccharides. Further- made of cells that are dead at functional maturity and, W more, the Michaelis–Menten constants (Km) of the shes’ hence, lack the cell contents on which many herbivorous animals thrive. Because wood is composed almost entirely of structural polysaccharides (e.g., lignocellulose), it is con- Communicated by I. D. Hume. sidered to be nutrient poor (Karasov and Martínez del Rio 2007). Thus, many wood-eating, or xylivorous, animals Electronic supplementary material The online version of this article (doi:10.1007/s00360-009-0383-z) contains supplementary (e.g., lower termites, beavers) require the aid of symbiotic material, which is available to authorized users. microorganisms in their gastrointestinal (GI) tracts to digest cellulose and make the energy in this compound available D. P. German · R. A. Bittong to the host (Prins and Kreulen 1991; Vispo and Hume Department of Zoology, University of Florida, Gainesville, FL, USA 1995). Indeed, xylivorous animals possess an expanded hindgut or cecum in which microbes reside and produce Present Address: cellulolytic enzymes to aid in the digestion of woody mate- D. P. German (&) rial (Prins and Kreulen 1991; Vispo and Hume 1995; Mo Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA et al. 2004). Because the conditions in this expanded e-mail: [email protected] hindgut are typically anaerobic, microbial endosymbionts 123 1026 J Comp Physiol B (2009) 179:1025–1042 operate under fermentative pathways, reducing glucose 2009). Furthermore, loricariids have long, thin-walled (and other monomers) to byproducts called short-chain intestines (Delariva and Agostinho 2001; German 2009b), fatty acids (SCFAs; e.g., acetate), which are then absorbed which suggests that they have high levels of intake of low- by the host animal and used to generate ATP (Bergman quality food (Sibly and Calow 1986; Horn and Messer 1990; Karasov and Martínez del Rio 2007). 1992; Karasov and Martínez del Rio 2007), such as detritus In 1993, Schaefer and Stewart described several new (Araujo-Lima et al. 1986). High intake equates to rapid gut species as part of a lineage of neotropical catWshes, genus transit and little endosymbiotic fermentation (Stevens and Panaque, which may possibly be xylivorous. The enlarged Hume 1998; Crossman et al. 2005; Karasov and Martínez teeth these animals use to scrape wood from the surface of del Rio 2007; German 2009a). fallen trees in the river, and the presence of wood as the Nelson et al. (1999) examined digestive enzyme activi- “only macroscopic material” in the Wshes’ GI tracts ties and cultured microbes from the GI tracts of Panaque intrigued the authors (Schaefer and Stewart 1993). Further- maccus, and an undescribed species of Pterygoplichthys more, xylivory evolved twice in loricariid catWshes, as a (formerly Liposarcus; Armbruster 2004), both of which clade in the genus Hypostomus (Armbruster 2003) is recog- they obtained via the aquarium trade. Nelson et al. were nized as wood-eating in addition to the Panaque (Fig. 1). able to isolate aerobic microbes with cellulolytic capabili- Both xylivorous clades are derived within the phylogeny, ties from the guts of the two species and measured cellulase but little is known of the digestive physiology of these activities in the Wshes’ GI tracts. From these results, Nelson Wshes, and whether they can digest cellulose from wood. et al. (1999) concluded that loricariids possess an endosym- The xylivorous catWshes belong to the Loricariidae, a biotic community in their guts capable of digesting cellu- diverse catWsh family (680 described species in 80 genera) lose under aerobic conditions. Conversely, German (2009b) endemic to the neotropics (Armbruster 2004). The diets of showed that Panaque nigrolineatus and Pterygoplichthys relatively few species of loricariids are known (Delariva disjunctivus passed wood through their guts in less than 4 h, and Agostinho 2001; Pouilly et al. 2003; de Melo et al. could not assimilate signiWcant amounts of cellulose from 2004; Novakowski et al. 2008; German 2009b) and appear wood and, hence, did not thrive on a woody diet in the lab- to include animal, plant, and detrital material from the oratory. What is clearly needed is an analysis of digestive benthos. Loricariids are known to consume morphic (e.g., tract function to better understand the digestive strategy of wood) and amorphic (i.e., unidentiWable colloidal material) the wood-eating catWshes. Do these catWsh GI tracts detritus (German 2009b). It is clear, however, that these function more like those of other xylivorous animals Wshes have undergone evolutionary rearrangements of jaw (Breznak and Brune 1994; Vispo and Hume 1995; Felicetti structure, allowing for diversity in feeding modes and tro- et al. 2000), with some mechanism for slowing the Xow of phic specialization (Schaefer and Lauder 1986; Lujan digesta and allowing microbes to ferment refractory Fig. 1 Partial phylogenetic H hypothesis for three tribes in the yp ostomini catWsh family Loricariidae Hypostomus cochliodon group (7)* (Armbruster 2004). Phylogeny based on parsimony analysis of 214 morphological characters. Hypostomus (20) Pter See Armbruster (2004) for yg statistical support. Genera in o Hemiancistrus (20) p bold include wood-eating lichthini species, and the asterisks (*) indicate genera from which Pterygoplichthys (14) * species were investigated in this study. Numbers in parentheses Panaque (small; 5) * indicate approximate number of taxa not shown Panaque (large; 3) * Ancistrini Pekoltia (2) Hypancistrus/Parancistrus (2) Six genera (7) Hemiancistrus/Pekoltia (3) Chaetostoma and others (30) Hemiancistrus sp. (1) 123 J Comp Physiol B (2009) 179:1025–1042 1027 polysaccharides (Clements and Raubenheimer 2006; Karasov hospitable to an anaerobic population of endosymbiotic and Martínez del Rio 2007), or are their guts more similar microorganisms, or whether the Wshes’ guts were aerobic, to those of other detritivorous Wshes (Horn and Messer as proposed by Nelson et al. (1999). Second, luminal carbo- 1992; Crossman et al. 2005; German 2009a), with rapid gut hydrate proWles and SCFA concentrations were measured transit, a reliance on endogenous digestive mechanisms along the GI tract to determine where nutrients were being and, hence, little digestion of refractory polysaccharides? hydrolyzed and absorbed, and where microbes might be These divergent digestive strategies not only feature most concentrated in the GI tract. If the Wsh were reliant on diVerences in digesta transit rate and gut morphology, but endosymbiont fermentation to gain energy from
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