Passiflora auriculata

P. auriculata is one of the two most common species of Passiflora in second growth and edge habitats at La Selva. The large yellow nectaries at the base of the leaf petiole and on the leaf blades are unique, and are very attractive to ants. P. auriculata plants frequently sprawl with many short branches but larger vines may be present with thick triangular or sometimes flattened stems. P. auriculata flowers are fairly small as are the dark purple or black fruits. The nectaries on the leaf blade may be distinctly yellow and may act as egg mimics to deter oviposition by Heliconius butterflies. Range: Nicaragua to Bolivia, Brazil and Venezuela. Wet forest from sea level to 1700 meters elevation. A member of section Auriculata, subgenus Decaloba, with principal diversity in the Amazon basin.

HCN measurements reveal that P. auriculata foliage produces small but variable amounts of HCN when crushed (0.01 to 1.0 μM HCN per gram of new leaves), with tiny seedling leaves ranging up to 10 μΜ/g. P. auriculata contains the simple monoglycoside cyclopentyl cyanogen Epivolkenin, with tiny amounts of other cyanogens present (Engler et al 2000). The 2 orders of magnitude range appears to be significant to many of the flea beetle species, and most plants with significant flea beetle feeding damage are at the lower end of the range. Rootlets, like seedling leaves, have 10 times larger amounts, ranging from .6 to 6 μM/g HCN (wet weight).

I investigated P. auriculata HCN variation in more detail by locating 11 widely spaced individual plants, each with multiple branches along a common stem. I collected three leaves from each branch, including a new leaf not yet fully expanded, a full-sized new leaf, and the oldest leaf. In 5 cases I could verify the common origin of each branch by tracing the stems downward and locating the connection, but in 6 other cases the stems ran under logs and debris and could not be followed. In those cases I judged that the spatial separation between plants was sufficient that I could assume a common connection. I did not use leaf appearance, maturity, or degree of shading as criteria for identifying connected branches. The results of over 100 measurements expressed on a log scale may be seen in Figure 5a. Within-species variation in HCN. The figure reveals average within-branch variation of about 0.7 log units (5x), between-branch variation of about .4 (2x), and a between-plant variation of about 1.0 (10x). See Figure 5d and charts below for more details. About half of the 100-fold variation in P. auriculata leaf HCN may be attributed to differences between plants, and the other half to variation among branches and leaves within a plant. It is interesting to note that I could not see any external differences between high- and low-HCN plants, other than the amount of flea beetle feeding damage. The latter was often inversely correlated with quantity of HCN (see chart below).

H. cydno, H. hecale and especially the specialist H. sara lay their eggs on P. auriculata at La Selva, the former species on the tendril tips and the latter laying her clutches of eggs on the shoot tips among the incipient leaves. If H. sara clutches escape parasitism by egg parasites (Trichogrammatidae and Scelionidae), the resulting 30-50 caterpillars can rapidly defoliate a plant. Measurements show that the larvae of the P. auriculata specialist H. sara do not release any detectable HCN while feeding on this plant.

This species is also eaten by several species of flea beetle, including the generalist Blue Flea Beetle (Monomacra violacea), the Yellow-legged Flea Beetle (Parchicola DF-2), and the Red-brown-white Flea Beetle (Ptocadica bifasciata). The black-tibia and the yellow tibia Parchicola species have also been observed on several occasions. The Striped Flea Beetle (Disonycha quinquelinata) was observed once on this plant. Pt. bifasciata eggs and larvae have been found on the leaves of the plant, as have the immature stages of Parchicola DF2. Pa. DF2 eggs are laid at the base of the plant amoung the surface rootlets or, alternatively, on the underside of leaves near the base of the plant. Flea beetles often "infest" individual P. auriculata plants for long periods (perhaps permanently) once a large patch of plant is found, but (unlike P. lobata) I have seldom seen patches die off or otherwise disappear. Perhaps the elevated amounts of cyanogenic glycosides provide some protection for the roots and stems.

I have confined M. violacea adults on P. auriculata in cages in the shadehouse, but no reproduction has occurred.


 

Heliconius sara eggs laid on P. auriculata shoot tip.
H. erato larva feeding on P. auriculata. H. erato also feeds on P. biflora and P. coriacea among other species in Passiflora subgenus Decaloba.
H. sara larvae feed in groups un the underside of P. auriculata leaves. Heliconius sara pupa, commonly found on or near P. auriculata vines.

 

Ptocadica bifasciata on P. auriculata. This flea beetle is also commonly found on P. biflora.
The Blue flea beetle Monomacra violacea is commonly found on P. auriculata.
P. auriculata flowers are not spectacular like some Passiflora.
P. auriculata plants usually produce many small flowers at once.
Here I measure zero parts per million (actually <0.3 ppm) of HCN produced by these rapidly feeding Heliconius sara caterpillars, eating leaves of Passiflora auriculata, a weakly cyanogenic species according to our measurements. Green fruits. The ripe fruits are dark purple with lots of black seeds. Not very palatable.
Note the beautiful black and yellow anthers. A commonly seen sight: auriculata holed by flea beetles. A Yellow-legged Flea Beetle (Parchicola DF2) may be seen in the center of the leaf.
Sometimes ants cover the leaves in order to get the nectar from the various glands. P. auriculata may be the best-protected Passiflora in terms of ant attendance. This Philaethria dido larva was feeding on P. auriculata. This is an unusual host plant record for this species, which normally feeds on P. vitifolia. P. dido is a green and black heliconiine.
Closeup of Yellow-legged Yellow flea beetle Parchicola DF2. This may be the smallest of the Passiflora-feeding flea beetles at La Selva. Note the huge "auriculate" nectaries on the petiole. Larva of the Riodenid butterfly Juditha molpe, drinking from nectary alongside Ectatomma ant. Many Riodenids are adapted to live with ants and are safe in their presence. J. molpe feeds on plants belonging to several families.
Larva of Ptocadica bifasciata, feeding on P. auriculata. The function of the protuberances on the back and sides is not known but may help in protection against ants and other predators. The head is hidden most of the time and so are the legs. Ectatomma tuberculatum ants feeding on P. auriculata nectaries. These ants guard their nectaries and grab nectary visitors as well as eating Heliconius caterpillars. Flea beetles seem relatively immune to their efforts at predation.
Agelaia cajennensis wasp (Hymenoptera: Vespidae) cutting up H. sara larva and forming into a "meat" ball to feed its larvae. This process of cutting up probably releases any HCN contained in the caterpillar's tissues. Black-tibia Flea Beetle (Parchicola "Black-tibia") was sitting for 5 days on this P. auriculata plant.

Right: Passiflora auriculata plants with substantial flea beetle feeding damage vs. those without damage: Comparison of HCN content in foliage. Note non-significant trend (p=.16) for flea beetle host plants to have reduced amounts of HCN production (about 50% less). HCN was measured from a single leaf on each plant.

 

 


Below: Analysis of variance of HCN produced by crushing 3 leaves from 37 branches of of P. auriculata (log μM/g). The 37 branches were taken from 11 individual plants. This graph shows the average HCN per plant and the standard errors of the means.  Plants vary significantly in average  μM/g HCN (ANOVA p<0.0001)

Mean quantity (μM/g) of HCN produced by crushing 3 leaves from 37 branches of of P. auriculata. The 37 branches were taken from 11 individual plants.  The bars represent standard error of the mean. After subtracting the average differences among plants, the remaining within-plant variation between branches is also significant (p=0.002).

 

On average I found no difference in HCN content between new (left) and older leaves (right) for P. auriculata.


HCN release after leaf crushing, measured in sealed 9.6 liter container. In this case to get enough material I crushed 8 new leaves. Peak release occurs at about 200 seconds, slow as compared with many other species. In addition the quantities released are easily measured but are very low.
Amount of HCN released by 12 leaves from a P. auriculata branch. This bimodal pattern with shallow peaks near the tip and as leaves mature can be seen in other species. Note that this branch was growing rapidly and was free of any signs of herbivory.
Another P. auriculata branch in the garden, growing rapidly and free from herbivory (black squares; even numbered leaves only). Sampling tissue from the even numbered leaves caused damage which could potentially unduce changes in HCN amount. This was measured the next day (green triangles; 24h). No change was seen except for leaves 2 (increase) and 12 (decrease). I also measured the alternate, odd numbered leaves (black X's). These measurement fell right on the line for the intact branch, signifying no change to those leaves. Finally, I sampled all 12 leaves the next day (the 48h symbols) and saw no evidence for long term induction.