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. 2017 Jul 18;12(7):e0181252.
doi: 10.1371/journal.pone.0181252. eCollection 2017.

Effects of prey, pitcher age, and microbes on acid phosphatase activity in fluid from pitchers of Sarracenia purpurea (Sarraceniaceae)

Carl S Luciano  1 , Sandra J Newell  1
Affiliations

Effects of prey, pitcher age, and microbes on acid phosphatase activity in fluid from pitchers of Sarracenia purpurea (Sarraceniaceae)

Carl S Luciano et al. PLoS One. .

Abstract

Carnivory in pitcher plants generally involves digestion of prey, by the plant itself, by symbionts, or both. While symbionts appear to be important in the digestion of prey in Sarracenia purpurea, the importance of pitcher-derived enzymes is less well documented. Our goal was to reduce microbial numbers in pitcher fluid in order to measure the acid phosphatase activity attributable to the pitchers themselves. Preliminary experiments indicated that various antibiotics were minimally effective at reducing microbial populations and that antibiotic-resistant microbes were easily cultured from pitcher fluid. Consequently, we measured the abundance of culturable microbes in every sample taken for the measurement of acid phosphatase activity. Pitchers fed with one sterilized ant had higher levels of acid phosphatase activity than unfed pitchers. Older pitchers were more responsive to feeding than young pitchers. Pitchers with high levels of microbes (on Day 5) had higher acid phosphatase activity than pitchers with low levels of microbes. However, fed pitchers were not more likely to have higher microbe levels and microbe levels were not related to pitcher age. When fluid samples from inside the pitcher were compared to appropriate controls incubated outside the pitcher, acid phosphatase activity was higher inside the pitcher. Results from the feeding experiments are consistent with a primary role of microbes in the digestion of prey in pitchers of S. purpurea. However, the relationship between pitcher age and enzyme activity is not a function of microbes in the pitcher fluid and may depend on enzymes produced by the plant. Our methods would not detect microbes embedded on the inner surface of the pitcher; and if they survived the alcohol rinse and antibiotics, we cannot rule out microbes as the source of the relationship between pitcher age and acid phosphatase activity.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Frequency distribution illustrating the number of pitchers with a given level of acid phosphatase activity (μg/mL) inside the pitcher on Day 5 of the experiment (AcP(5)).
Fed pitchers (black bars) exhibited a more skewed distribution with higher levels of acid phosphatase activity than unfed pitchers (gray bars).
Fig 2
Fig 2. Regression analysis of log acid phosphatase activity across pitcher age (d) for fed and unfed pitchers.
Both fed and unfed pitchers exhibited an increase in acid phosphatase activity with increasing pitcher age, with a greater increase in the fed pitchers. Pitcher age accounted for almost 39% of variation in enzyme activity in fed pitchers and just under 17% of the variation in enzyme activity in unfed pitchers.
Fig 3
Fig 3. Means (± 1 SE) of the log of acid phosphatase activity measured on Day 5 (Log AcP(5)) for fed and unfed pitchers in four age groups.
Fed pitchers exhibited a trend of increasing enzyme activity with pitcher age. Homogeneous subsets identified by Tukey HSD are labeled with the same letter. Sample sizes for Fed are: Age 0–6, n = 13, Age 14–20, n = 21, Age 26–30, n = 19, Age 40+, n = 3; and for Unfed are: Age 0–6, n = 14, Age 14–20, n = 14, Age 26–30, n = 14, Age 40+, n = 4.
Fig 4
Fig 4. Initial acid phosphatase activity (AcP(0)) (μg/mL) subtracted from final acid phosphatase activity (AcP(5)) μg/mL) in fed (dark gray bars) and unfed (light gray bars) pitchers for three age groups of pitchers.
Differences (mean ± 1 SE) increased with pitcher age, to a greater degree in fed pitchers than in unfed pitchers. (Samples sizes are: Age 0–6, Unfed, n = 14, Fed, n = 13; Age 14–20, Unfed, n = 14, Fed, n = 21; Age 26+, Unfed, n = 18, Fed, n = 22).
Fig 5
Fig 5. Regression analysis of log acid phosphatase activity on Day 5 across pitcher age (d) for fed pitchers separated on the basis of microbe levels on Day 5 (Microbes(5)), taken from samples of pitcher fluid.
Enzyme activity increased with pitcher age in all three microbe levels. The amount of variation explained by pitcher age (R2) decreased with increasing microbe levels.
Fig 6
Fig 6. Mean acid phosphatase activity of fluid inside the pitcher, measured on Day 5 (Inside Pitcher AcP(5)), was significantly higher than paired controls.
Samples taken from each pitcher on Day 0 were incubated outside the pitcher, and acid phosphatase activity was measured on Day 5 (Paired Outside AcP(5)). Paired Outside AcP(5) and Inside Pitcher AcP(5) are sorted by feeding status and microbe levels inside the pitcher on Day 5 (Microbes (5)). The asterisks represent a statistically significant difference between Paired Outside AcP(5) and Inside Pitcher AcP(5) using paired t-tests, * = P < 0.01, ** = P < 0.001. Paired t-tests were performed on log-transformed data, and antilogs of means are represented with 95% confidence intervals. (Sample sizes are: Unfed, Low Microbes (5), n = 35; Unfed, High Microbes (5), n = 11; Fed, Low Microbes (5), n = 36; Fed, High Microbes (5), n = 20).
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Substances

Grants and funding

The authors CSL and SJN received funding from the IUP Senate (http://www.iup.edu/senate/committees/research/) and the IUP School of Graduate Studies (http://www.iup.edu/graduatestudies/) to support this work but no specific grant numbers were associated with the funding. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.