Philcoxia: The plant that ate the nematode on subterranean leaves

Could it be? Do we have confirmation of a new genus of carnivorous plants? Possibly. The small genus Philcoxia, which is endemic to Brazil and consists of only three diminutive species, was only just described in 2000. Even in the original description of the plants, authors were noting stalked glands and sticky leaves with later studies observing dead nematodes covering the leaves. These were just hints at the possibility that the plants were deriving some benefit from trapping and killing the wee-beasties and thus might be true carnivorous plants. Definitions vary, but for a plant to be considered carnivorous, it must be demonstrated that the plant has adaptations to (sometimes) lure, trap, and digest prey, absorb the nutrients, and crucially, derive some benefit from it.

Philcoxia minensis - source: Pereira et al., 2012.

But let's back up here. What did we know before this study? Philcoxia grows in nutrient-poor sandy soils, oddly holding its leaves at or just below the ground surface so that the leaves are often covered with sand grains. They have poor root systems, aren't very tall even when in flower, and usually have 5-10 leaves on each plant. When the leaves were examined closely, they were covered in dead nematodes, captured by the sticky secretions among the stalked glands on the upper surface of the leaf.

Sounding familiar yet? To anyone that's acquainted with the other flypaper-type carnivorous plant traps like the sundews (Drosera) and butterworts (Pinguicula), the above description checks all of the boxes for what you'd look for in a carnivorous plant: the need to derive nutrients from sources other than soil, sticky leaves with stalked glands, often ephemeral habits. Most important until this point was the direct observation of nematode prey, published in a 2007 article. The poor nematodes didn't know what hit them; they were mindlessly searching for a brunch of bacteria and they ended up on the menu instead. The 2007 study tested for a common digestive enzyme, proteases, that are often a hallmark of carnivorous plants but detected none, noting, of course, that absence of proteases did not preclude the possibility that Philcoxia was carnivorous after all.

Typical habitat of P. minensis at Serra do Cabral, Minas Gerais, Brazil.
Source: Fritsch et al., 2007

The present study by Pereira et al. (2012), published online ahead of print in PNAS, finally digs deeper and provides us with more experimental evidence. The authors went out into the field, collected plants of P. minensis, and acclimated them to the greenhouse. In what has become standard procedure for determining movement of nutrients from prey to plant, the authors fed 15N-labeled C. elegans nematodes to the plant and left it for 48 hours. The presence of the isotope in the plants cleared of all nematodes after that period of digestion easily indicates that the source of the 15N was the nematode. Compared to controls where no nematodes or nematodes reared without the isotope were fed to the plant, a significant 15% of the isotope originally found in the prey was now found in the leaf biomass after 48 hours. The increase in 15N was associated with an overall increase in nitrogen content of the leaf. My only criticism here is that sample size for all treatments was relatively low at n = 8 and thus the standard error bars are large, though I fully recognize that this is a difficult species to cultivate. I'm also likely spoiled by my time in a microbiology lab where sample size was almost never a problem. As preliminary evidence, this is quite promising! (Out of curiosity, I would have loved to see data on 15N from parts of the plant other than the leaves, since transport of nutrients would be efficient in that 48 hour period.)

While absorption of labeled nutrients from nematode prey is an indication of foliar uptake of nutrients, Pereira et al. conclude that this is also evidence for digestion via the plant's own digestive enzymes. (As an aside, I note that foliar absorption of mineral nutrients is common in plants.) This is a bigger leap from evidence to conclusion and isn't well supported. What we know from Pereira et al. is that the leaves do produce lots of phosphatases, another one of the digestive enzymes that indicates carnivorous activity. It's an easy inferential leap to make from presence of phosphatases and assumed absence of bacterial activity on the leaf's surface in the greenhouse experiment that could otherwise explain the mineralization instead of direct action of the plant. It would be difficult, but ideally Philcoxia should be grown in tissue culture in the absence of bacteria, then be fed the isotope-labeled nematodes for the most convincing data to support the idea of digestion via the plant's enzymes alone.

A group of P. minensis leaves in the sand.
Source: Pereira et al., 2012

The authors also measured neighboring noncarnivorous plants in the field and noted that Philcoxia has a significantly higher nitrogen and phosphorous content. This begins to address the "benefit" part of the definition of carnivory. The higher nutrient content may be an indication of a benefit from the nematodes and the authors note that further investigation, including direct observation of photosynthetic rates, is already underway. More convincing might be an clear increase in biomass or seed set, but with such small plants, elevated photosynthetic rates might be a better measure.

In summary, Philcoxia traps and kills nematodes on subterranean leaves, possibly digests it with enzymes such as phosphatases produced by the plant, absorbs the nutrients, and possibly derives a benefit from the prey in that the plants have higher nutrient content than their noncarnivorous neighbors in the unforgiving and nutrient-poor environment. What's conspicuously missing here is evidence of a lure or attractant. What's the normal concentration of nematodes in the sand surrounding the plant? Is their capture accidental or are they drawn to their death on the subterranean leaves? These questions were also identified by the authors as avenues for further research. I look forward to these!

In my assessment, with further data we can certainly add this genus to the ranks of true carnivorous plants. As Pereira et al. mentioned, this has implications for our understanding of the number of times carnivory has evolved among plants since Philcoxia belongs to the plantain family (Plantaginaceae), which previously counted no known carnivorous plants among its members. Depending on which you include, this means that plant carnivory has evolved at least 7 times independently, a fact I find amazing to ponder.

(h/t to Paul Riddell of the Texas Triffid Ranch for originally pointing me to this new research. Thanks!)

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References:

Pereira, CG, Almenara, DP, Winter, CE, Fritsch, PW, Lambers, H, & Oliveira, RS (2012). Underground leaves of Philcoxia trap and digest nematodes. Proc. Natl. Acad. Sci. USA : 10.1073/pnas.1114199109

Fritsch, PW, Almeda, F, Martins, AB, Cruz, BC, & Estes, D (2007). Rediscovery and Phylogenetic Placement of Philcoxia minensis (Plantaginaceae), with a Test of Carnivory Proc. CA Acad. Sci., 58, 447-467

Taylor, P., Souza, V., Giulietti, A., & Harley, R. (2000). Philcoxia: A New Genus of Scrophulariaceae with Three New Species from Eastern Brazil Kew Bulletin, 55 (1), 155-163 DOI: 10.2307/4117770