Holly trees play a significant role in the beliefs and traditions of the season. To the Romans, hollies were the trees of the god Saturn and wreaths of holly were given as gifts during his holiday, Saturnalia. In Celtic legends, the evergreen hollies with their beautiful red berries announced the triumph of the Holly King during winter over the Oak King, who ruled the forest with his green leaves in summer. For Christians, the pointed leaves of holly are associated with the crown of thorns worn by Jesus and bright red holly berries symbolize drops of his blood. For a bug guy, this is the season to marvel at a pair of fascinating flies whose lives are intimately tied to our beautiful native holly.
On my neighbor's splendid American holly, red fruits intermingle with deep green leaves. Some leaves have unusual sinuous trails on their surface. Within the trails are the larvae of small flies, the young of the native holly leafminer. Back in the warmth of spring, the adult stage of the female native holly leafminer, a small black fly, pierced the holly leaf with a structure on the tip of its abdomen called an ovipositor. This egg-laying appendage deposited an egg through the tough leaf surface into the soft tissue beneath. Upon hatching, the tiny larva consumed nutritious cells of the holly leaf and snaked its way through the leaf, enlarging the trail as it grew. In the dead of winter the larva rests, but on warm days during winter and early spring the leafminer will continue to feed until it completes development and forms a pupa in spring.
See the tiny yellow leafminer larva near the tip of the forceps on the inside layer of leaf epidermis.
Before the larva changes into a pupa, it cuts a small window in the surface of the leaf to enable the adult fly to escape after pupation. The emergence of the adult fly is timed to coincide with the appearance of tender new holly leaves in spring. In addition to laying eggs, the female holly leafminer uses her sharp ovipositor to poke holes in the leaf's surface. These small holes exude droplets of sap, thereby providing a source of food for the hungry female. Leaves with many feeding holes are often curled or puckered. A horticulturalist once told me that these holes were caused by holly leaves with sharp spines bumping into one another, but now we know differently.
The beautiful bright red berries of American holly attract many fascinating feathered friends such as mocking birds, blue jays, and cardinals, to a winter feast. The berries provide a nutritious meal, and in return the birds distribute the holly to new places by depositing seeds in their droppings. While photographing the native holly leafminer, I spotted several holly berries that were distinctly green rather than scarlet red. Inside these fruits were tiny yellow maggots, larvae of the holly berry midge. Back in the spring when hollies were in bloom, the adult holly berry midge, a small mosquito-like fly, deposited eggs into the developing fruit of holly. These eggs hatched into larvae that fed within the berry. During the past growing season, the maggots consumed tissue of the fleshy fruit. In winter, larval development slows, but when the warmth of spring returns these maggots complete development and become pupae, from which emerge small midges that mate and deposit eggs into newly developing berries, thereby completing the cycle of life.
Inside the holly berry, tiny holly berry midge larvae consume juicy plant cells. At less than 2 mm in length it’s hard to tell which end is which. In this video the head end is to the left and the rear end is to the right.
For a small maggot, life in a holly berry is precarious. Its fate is tied to a red berry that advertises "eat me", and hungry birds and squirrels happily oblige. These frugivores could literally eat the holly berry midge out of house and home. However, the larva of the holly berry midge has a clever trick to lessen its risks of disappearing along with its fruity home down the gullet of a bird. Berries infested by holly berry midge fail to turn red as do normal holly berries. The midge and an associated fungus prevent formation of bright red pigments by the berry. Infested berries remain green all winter. Through a series of detailed observations, researchers found that green holly berries were much less likely to be eaten by squirrels and birds than red berries on the same tree. By preventing the berry from turning red, holly berry midge has found a way to avoid the attention of fruit eating critters, thereby enhancing its chances for survival. So, as you deck your halls with boughs of holly, should you spy a green berry you will understand why green is good for the cunning holly berry midge.
During this festive season, I always bring fresh holly branches into my home and, with any luck, leaves adorned by holly leafminers and festive green berries infused with holly berry midge always make the season even jollier.
Bug of the Week wishes you a very jolly Holiday Season
and a spectacular New Year!
We thank John Davidson for providing the inspiration and images for this week’s episode. Four fascinating references, “Population regulation of the native holly leafminer, Phytomyza ilicicola Loew (Diptera: Agromyzidae), on American holly” by Daniel A. Potter; “Seasonal allocation of defense investment in Ilex opaca Ation and constraints on a specialist leafminer“ by D.A. Potter and T.W. Kimmerer; the book “Managing Insects and Mites on Woody Landscape Plants” by John Davidson and Michael Raupp; and the interesting article “Selective Avoidance by Vertebrate Frugivores of Green Holly Berries Infested with a Cecidomyiid Fly (Diptera: Cecidomyiidae)” by Vera Krischik, Eric S. McCloud and John A. Davidson, were used to prepare this episode.