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Capture of mammal excreta by Nepenthes is an effective heterotrophic nutrition strategy

Cross AT, van der Ent A, Wickmann M, Skates LM, Sumail S, Gebauer G, et al.

Ann Bot, 2022 Dec 31;130(7):927-938.
PMID: 36306274 DOI: 10.1093/aob/mcac134

BACKGROUND AND AIMS: While isotopic enrichment of nitrogen (15N) and carbon (13C) is often used to determine whether carnivorous plant species capture and assimilate nutrients from supplemental sources such as invertebrate prey or mammal excreta (heterotrophic nutrition), little is known about how successful the different strategies deployed by carnivorous plants are at obtaining supplemental nutrition. The collection of mammalian faeces by Nepenthes (tropical pitcher plants) is the result of a highly specialized biological mutualism that results in heterotrophic nitrogen gain; however, it remains unknown how effective this strategy is in comparison to Nepenthes species not known to collect mammalian faeces.
METHODS: We examined how isotopic enrichment varied in the diverse genus Nepenthes, among species producing pitchers for invertebrate capture and species exhibiting mutualisms for the collection of mammal excreta. Enrichment factors were calculated from δ15N and δ13C values from eight Nepenthes species and naturally occurring hybrids along with co-occurring reference (non-carnivorous) plants from three mountain massifs in Borneo: Mount Kinabalu, Mount Tambuyukon and Mount Trus Madi.
RESULTS: All Nepenthes examined, except N. edwardsiana, were significantly enriched in 15N compared to co-occurring non-carnivorous plants, and 15N enrichment was more than two-fold higher in species with adaptations for the collection of mammal excreta compared with other Nepenthes.
CONCLUSIONS: The collection of mammal faeces clearly represents a highly effective strategy for heterotrophic nitrogen gain in Nepenthes. Species with adaptations for capturing mammal excreta occur exclusively at high elevation (i.e. are typically summit-occurring) where previous studies suggest invertebrate prey are less abundant and less frequently captured. As such, we propose this strategy may maximize nutritional return by specializing towards ensuring the collection and retention of few but higher-value N sources in environments where invertebrate prey may be scarce.

Matched MeSH terms: Carnivory*
Fulltext Proteomic analysis of pitcher fluid from Nepenthes × ventrata

Wan Zakaria WNA, Aizat WM, Goh HH, Noor NM

Data Brief, 2018 Apr;17:517-519.
PMID: 29876422 DOI: 10.1016/j.dib.2018.01.037

The carnivorous plants of genus Nepenthes produce unique pitchers containing secretory glands, which secrete proteins into the digestive fluid. We investigated protein profile in the pitcher fluid during the first three days of opening to understand carnivory trait of Nepenthes × ventrata. The proteome analysis of pitcher fluid from N. × ventrata was performed by label-free quantitative liquid chromatography mass spectrometry (nLC-MS/MSALL). Raw MS data have been deposited to the ProteomeXchange with identifier PXD007251. This dataset allows the identification and quantification of proteins from pitcher fluids to elucidate proteins involved in carnivory physiology of Nepenthes species.

Matched MeSH terms: Carnivory
Fulltext Four New Species of Nepenthes L. (Nepenthaceae) from the Central Mountains of Mindanao, Philippines

Gronemeyer T, Coritico F, Wistuba A, Marwinski D, Gieray T, Micheler M, et al.

Plants (Basel), 2014;3(2):284-303.
PMID: 27135505 DOI: 10.3390/plants3020284

Together with the islands of Sumatra (Indonesia) and Borneo (Indonesia, Malaysia), the Philippines are the main center of diversity for carnivorous pitcher plants of the genus, Nepenthes L. Nepenthes are the largest of all carnivorous plants, and the species with the biggest pitchers are capable of trapping and digesting small amphibians and even mammals. The central cordillera of Mindanao Island in the south of the Philippines is mostly covered with old, primary forest and is the largest remaining cohesive, untouched area of wilderness in the Philippines. In a recent field exploration of two areas of the central cordillera, namely Mount Sumagaya and a section of the Pantaron range, four new taxa of Nepenthes were discovered. These four remarkable new species, N. pantaronensis, N. cornuta, N. talaandig and N. amabilis, are described, illustrated and assessed.

Matched MeSH terms: Carnivory
Interspecific variation in prey capture behavior by co-occurring Nepenthes pitcher plants: evidence for resource partitioning or sampling-scheme artifacts?

Chin L, Chung AY, Clarke C

Plant Signal Behav, 2014;9(1):e27930.
PMID: 24481246

Pitcher plants of the genus Nepenthes capture a wide range of arthropod prey for nutritional benefit, using complex combinations of visual and olfactory signals and gravity-driven pitfall trapping mechanisms. In many localities throughout Southeast Asia, several Nepenthes different species occur in mixed populations. Often, the species present at any given location have strongly divergent trap structures and preliminary surveys indicate that different species trap different combinations of arthropod prey, even when growing at the same locality. On this basis, it has been proposed that co-existing Nepenthes species may be engaged in niche segregation with regards to arthropod prey, avoiding direct competition with congeners by deploying traps that have modifications that enable them to target specific prey types. We examined prey capture among 3 multi-species Nepenthes populations in Borneo, finding that co-existing Nepenthes species do capture different combinations of prey, but that significant interspecific variations in arthropod prey combinations can often be detected only at sub-ordinal taxonomic ranks. In all lowland Nepenthes species examined, the dominant prey taxon is Formicidae, but montane Nepenthes trap few (or no) ants and 2 of the 3 species studied have evolved to target alternative sources of nutrition, such as tree shrew feces. Using similarity and null model analyses, we detected evidence for niche segregation with regards to formicid prey among 5 lowland, sympatric Nepenthes species in Sarawak. However, we were unable to determine whether these results provide support for the niche segregation hypothesis, or whether they simply reflect unquantified variation in heterogeneous habitats and/or ant communities in the study sites. These findings are used to propose improvements to the design of field experiments that seek to test hypotheses about targeted prey capture patterns in Nepenthes.

Matched MeSH terms: Carnivory
Biological aspects of channa limbata(cuvier, 1831) in ta bo - huai yai wildlife sanctuary, Phetchabun province, Thailand

Khoomsab K, Wannasri S

Sains Malaysiana, 2017;46:851-858.

The biological aspects of Channa limbata were studied between November 2013 and October 2014. A total of 346 fish specimens, 185 male and 161 female, were collected from Ta Bo, Huai Yai Wildlife Sanctuary, Phetchabun Province, Thailand. Specimens range from 7.3-17.2 cm in length with body weight 8-31 g; sex ratio between males and females was 1: 0.7. The length (L), weight (W) relationship for mixed sexes was W = 0.2064 L1.85 (R2=0.90). Gonadosomatic indices for males and females were measured monthly and varied from 0.21-0.65% and 1.96-3.74%, respectively. Condition factors for males and females ranged between 0.54 - 2.20 and 0.58 - 2.72, respectively, with fecundity range 956 to 4,652 eggs in females. Fecundity (F) to weight relationship was F = 189.53 W0.59 (R2 = 0.71) and fecundity to length relationship was F = 68.82 L1.15 (R2 = 0.77). The ratio between the intestine length and total length was 1:2, indicating that C. limbata was a carnivorous feeder. Analysis of the stomach contents gave 84% insects and 16% aquatic weed. These results can be applied to conserve efforts to prevent the extinction of C. limbata in protected areas.

Matched MeSH terms: Carnivory
Fulltext First molecular data and the phylogenetic position of the millipede-like centipede Edentistoma octosulcatum Tömösváry, 1882 (Chilopoda: Scolopendromorpha: Scolopendridae)

Vahtera V, Edgecombe GD

PLoS One, 2014;9(11):e112461.
PMID: 25389773 DOI: 10.1371/journal.pone.0112461

Edentistoma octosulcatum Tömösváry, 1882, is a rare, superficially millipede-like centipede known only from Borneo and the Philippines. It is unique within the order Scolopendromorpha for its slow gait, robust tergites, and highly modified gizzard and mandible morphology. Not much is known about the biology of the species but it has been speculated to be arboreal with a possibly vegetarian diet. Until now its phylogenetic position within the subfamily Otostigminae has been based only on morphological characters, being variably ranked as a monotypic tribe (Arrhabdotini) or classified with the Southeast Asian genus Sterropristes Attems, 1934. The first molecular data for E. octosulcatum sourced from a newly collected specimen from Sarawak were analysed with and without morphology. Parsimony analysis of 122 morphological characters together with two nuclear and two mitochondrial loci resolves Edentistoma as sister group to three Indo-Australian species of Rhysida, this clade in turn grouping with Ethmostigmus, whereas maximum likelihood and parsimony analyses of the molecular data on their own ally Edentistoma with species of Otostigmus. A position of Edentistoma within Otostigmini (rather than being its sister group as predicted by the Arrhabdotini hypothesis) is consistently retrieved under different analytical conditions, but support values within the subfamily remain low for most nodes. The species exhibits strong pushing behaviour, suggestive of burrowing habits. Evidence against a suggested vegetarian diet is provided by observation of E. octosulcatum feeding on millipedes in the genus Trachelomegalus.

Matched MeSH terms: Carnivory/physiology
A phylogenomic analysis of Nepenthes (Nepenthaceae)

Murphy B, Forest F, Barraclough T, Rosindell J, Bellot S, Cowan R, et al.

Mol Phylogenet Evol, 2020 03;144:106668.
PMID: 31682924 DOI: 10.1016/j.ympev.2019.106668

Nepenthaceae is one of the largest carnivorous plant families and features ecological and morphological adaptations indicating an impressive adaptive radiation. However, investigation of evolutionary and taxonomic questions is hindered by poor phylogenetic understanding, with previous molecular studies based on limited loci and taxa. We use high-throughput sequencing with a target-capture methodology based on a 353-loci, probe set to recover sequences for 197 samples, representing 151 described or putative Nepenthes species. Phylogenetic analyses were performed using supermatrix and maximum quartet species tree approaches. Our analyses confirm five Western outlier taxa, followed by N. danseri, as successively sister to the remainder of the group. We also find mostly consistent recovery of two major Southeast Asian clades. The first contains common or widespread lowland species plus a Wallacean-New Guinean clade. Within the second clade, sects. Insignes and Tentaculatae are well supported, while geographically defined clades representing Sumatra, Indochina, Peninsular Malaysia, Palawan, Mindanao and Borneo are also consistently recovered. However, we find considerable conflicting signal at the site and locus level, and often unstable backbone relationships. A handful of Bornean taxa are inconsistently placed and require further investigation. We make further suggestions for a modified infra-generic classification of genus Nepenthes.

Matched MeSH terms: Carnivory
Transcriptomic and Proteomic Analyses of Nepenthes ampullaria and Nepenthes rafflesiana Reveal Parental Molecular Expression in the Pitchers of Their Hybrid, Nepenthes × hookeriana

Zulkapli MM, Ab Ghani NS, Ting TY, Aizat WM, Goh HH

Front Plant Sci, 2020;11:625507.
PMID: 33552113 DOI: 10.3389/fpls.2020.625507

Nepenthes is a genus comprising carnivorous tropical pitcher plants that have evolved trapping organs at the tip of their leaves for nutrient acquisition from insect trapping. Recent studies have applied proteomics approaches to identify proteins in the pitcher fluids for better understanding the carnivory mechanism, but protein identification is hindered by limited species-specific transcriptomes for Nepenthes. In this study, the proteomics informed by transcriptomics (PIT) approach was utilized to identify and compare proteins in the pitcher fluids of Nepenthes ampullaria, Nepenthes rafflesiana, and their hybrid Nepenthes × hookeriana through PacBio isoform sequencing (Iso-Seq) and liquid chromatography-mass spectrometry (LC-MS) proteomic profiling. We generated full-length transcriptomes from all three species of 80,791 consensus isoforms with an average length of 1,692 bp as a reference for protein identification. The comparative analysis found that transcripts and proteins identified in the hybrid N. × hookeriana were more resembling N. rafflesiana, both of which are insectivorous compared with omnivorous N. ampullaria that can derive nutrients from leaf litters. Previously reported hydrolytic proteins were detected, including proteases, glucanases, chitinases, phosphatases, nucleases, peroxidases, lipid transfer protein, thaumatin-like protein, pathogenesis-related protein, and disease resistance proteins. Many new proteins with diverse predicted functions were also identified, such as amylase, invertase, catalase, kinases, ligases, synthases, esterases, transferases, transporters, and transcription factors. Despite the discovery of a few unique enzymes in N. ampullaria, we found no strong evidence of adaptive evolution to produce endogenous enzymes for the breakdown of leaf litter. A more complete picture of digestive fluid protein composition in this study provides important insights on the molecular physiology of pitchers and carnivory mechanism of Nepenthes species with distinct dietary habits.

Matched MeSH terms: Carnivory
The capacity for long-chain polyunsaturated fatty acid synthesis in a carnivorous vertebrate: Functional characterisation and nutritional regulation of a Fads2 fatty acyl desaturase with Δ4 activity and an Elovl5 elongase in striped snakehead (Channa striata)

Kuah MK, Jaya-Ram A, Shu-Chien AC

Biochim. Biophys. Acta, 2015 Mar;1851(3):248-60.
PMID: 25542509 DOI: 10.1016/j.bbalip.2014.12.012

The endogenous production of long-chain polyunsaturated fatty acids (LC-PUFA) in carnivorous teleost species inhabiting freshwater environments is poorly understood. Although a predatory lifestyle could potentially supply sufficient LC-PUFA to satisfy the requirements of these species, the nutrient-poor characteristics of the freshwater food web could impede this advantage. In this study, we report the cloning and functional characterisation of an elongase enzyme in the LC-PUFA biosynthesis pathway from striped snakehead (Channa striata), which is a strict freshwater piscivore that shows high deposition of LC-PUFA in its flesh. We also functionally characterised a previously isolated fatty acyl desaturase cDNA from this species. Results showed that the striped snakehead desaturase is capable of Δ4 and Δ5 desaturation activities, while the elongase showed the characteristics of Elovl5 elongases. Collectively, these findings reveal that striped snakehead exhibits the genetic resources to synthesise docosahexaenoic acid (DHA; 22:6n-3) from eicosapentaenoic acid (EPA; 20:5n-3). Both genes are expressed at considerable levels in the brain and the liver. In liver, both genes were up-regulated by dietary C18 PUFA, although this increase did not correspond to a significant rise in the deposition of muscle LC-PUFA. Brain tissue of fish fed with plant oil diets showed higher expression of fads2 gene compared to fish fed with fish oil-based diet, which could ensure DHA levels remain constant under limited dietary DHA intake. This suggests the importance of DHA production from EPA via the ∆4 desaturation step in order to maintain an optimal reserve of DHA in the neuronal tissues of carnivores.

Matched MeSH terms: Carnivory