Torrey Pines Docent Society 2019

Notes on Plant Galls and Witches’ Broom

Galls are abnormal growth of plant tissue that can be induced by insects, mites, nematodes (tiny round worms), fungi, or bacteria. We find them most easily on leaves and stems, but they can occur on any other parts of a plant, down to the roots. Most gall- inducing organisms are specific with the choice of host plants. Each organism induces galls with characteristic morphology. In most cases, the growth of the gall does not harm or kill the host plant. If so, the relationship can be described as a commensalism. The gall-inducing organism is benefited by the protection and food provided by the gall housing. These notes are divided into three parts. First is a quick reference to the most common galls that are observed with plants in TPSNR. The second part goes into some of the details of the organisms. The last part is on witches’ broom, another kind of abnormal plant growth.

Part I. Field Guide

In this part, we cover some of the most common plants galls that can be found in TPSNR, including the Extension and the marsh trail. The identification is by the gall itself; we can hardly see the tiny gall-inducing insects. For images of these insects, we have to use websites (see Bibliography).

Fig. 1. An oak apple gall on a Nuttall's scrub oak. This one is about 30 mm in diameter.

1 Oak Galls All oaks can bear galls and they may appear anywhere, from leaves, to petioles, branches, acorns, flower spikes (catkins), and even roots. The most eye-catching ones are oak apple galls on branches. They vary from about 6 mm to 40 mm in diameter. They very briefly turn an apple-like red (Fig. 1). Very soon, this fresh gall will dry up and turn brown. On the Nuttall's scrub oak (Quercus dumosa Nutt.), these galls are induced by the California gall wasp (Andricus quercuscalifornicus). Fig. 2. Half-dried oak galls induced by the Beaked Twig gall wasp on Nuttall's scrub Wasps, together with ants, bees and sawflies, oak. This one is about 12 mm in diameter. are in the insect order Hymenoptera. Within this order, gall wasps are in the family Cynipidae,1 which is quite large. There are some 800 species just in North America. These cynipid gall wasps are tiny. The adults usually grow to just several millimeters long. Thus they are also called gallflies because of the size, perhaps in comparison to the small fruit flies. Each gall-inducing species infects different parts of a plant and generates galls with characteristic size, shape, and color that also can depend on the season (more on this later with their life cycles). In fact, we usually identify an inducer by the gall characteristics. For example, another detachable gall that can be found on the scrub oak is induced by the Beaked Twig gall wasp (Disholcaspis plumbella), also a Cynipid. The galls induced by this wasp have whitish spots resembling polka dots (Fig. 2). As tempting as it may be from the outside, the inside of an oak apple gall is anything but appetizing (Fig. 3). If we cut one open, what we find are insect larvae eating up rotting plant tissue. A gall with multiple larvae with each occupying its own cavity, also called a chamber, is called polythalamous, and is monothalamous when there is just one cavity. Oak apple gall is polythalamous even though it is not clear in Fig. 3. What is evident is that the larvae have eaten up just about half of this gall. This fresh oak apple gall was still spongy and juicy (see the drippings in Fig. 3). Like the rest of the oak plant, the liquid is rich in tannic acid, which can be used to make ink (see Part II). The acid is also antibacterial and astringent, meaning that it causes the contraction of the skin and thus reduces bleeding. The Kumeyaay sliced up a fresh oak gall and applied the liquid on sores. After the larvae pupate and subsequently grow into adults, each wasp punches a hole

1 The root of the name is from the Latin cyniphes, which is derived from the Ancient Greek kníps, referring to some “stinging insects” that live under the bark of trees.

2 through the wall and emerges from the gall. The tiny holes, about 1 mm in diameter, are an indication on how small the wasps are. (See the dried galls in the Lodge display drawers.)

Fig. 3. Section of an oak apple gall, roughly 30 mm diameter, from Nuttall's scrub oak.

Fig. 4. A stem gall induced by the Irregular Spindle gall wasp on Nuttall's scrub oak. This one is about 25 mm long.

Fig. 5. A leaf gall induced by the Midrib gall Some cynipid gall wasps induce galls that wasp on Nutall’s scrub oak. appear as swellings of stems and branches. These are called integral galls as opposed to the detachable oak apple galls. On the Nuttall's scrub oak, these oak stem galls are induced by the Irregular Spindle gall wasp, Andricus chrysolepidicola (Fig. 4). The multiple pinholes, about 1 mm in diameter, indicate that this cynipid wasp also makes polythalamous galls. While oak leaf galls are not as conspicuous as apple galls, oak leaf abnormalities are very common. On the Nuttall's scrub oak, they can be caused by the Midrib gall wasp, Neuroterus washingtonensis, another cynipid gall wasp (Fig. 5).

3 All the cynipid gall wasps mentioned here also induce galls in other white oaks, which include the Valley oak (Quercus lobata) father up north, and the California scrub oak (Quercus berberidifolia) a bit farther inland. There are other gall inducing insects, but with the local oaks, we can always start our guess with cynipid gall wasps.

Coyote Brush Midge Galls On the Coyote brush, Baccharis pilularis, we often find small globular (or ball- Fig. 6. A gall, about 12 mm in diameter, shaped) galls that grow to around 10 mm in on the Coyote brush induced by the bud gall diameter at the tip of the branches (Fig. 6). midge. Often there are short leaflets protruding from them. They first appear as whitish but will turn green or even purple in time. As they turn red or purple, the surface of the gall tends to become lumpy. These galls are induced by the Coyote brush bud gall midge, Rabdophaga californica (formerly classified under Rhabdophaga). Midges belong to the suborder Nematocera of flies (order Diptera), and they are small, about 2 to 3 mm in length. They have long skinny legs and antennae like that of mosquitoes. Gall midges are in one of the Nematoceran families, Cecidomyiidae.2 They are also called gall gnats because they are tiny.

Fig. 7. A sectioned Coyote brush bud gall showing multiple insect larvae (not too clear Fig. 8. A dried Coyote brush bud gall, about in the photo), each occupying its own cavity. 15 mm wide, with two smaller ones above. They all have roughly 1 mm pinholes punched through by the adult midges.

2 Cannot trace the etymology of the entire term, but cecidology is the study of plant galls.

4 Even though the bud galls are small, there are multiple larvae living inside. These galls are polythalamous. Each larva makes its own cavity. A dissected gall would show several tiny larvae inside (Fig. 7), but a more telling sign is from the number of pinholes punched out by the emerged adults in a desiccated gall (Fig. 8).

Fig. 9. White sage leaf galls induced by a gall midge but here at the base of petioles. These are about 5 mm in height.

Sage Leaf Galls Both the white sage (Salvia apiana) and the black sage (Salvia mellifera) may have leaf galls. They are caused by the sage leaf gall midge, Rhopalomyia audibertiae, which is also in the family of Cecidomyiidae.3 Fig. 9 shows the characteristic urn- shaped galls on a white sage, and in this particular case, the galls are at the base of the petiole instead of on a leaf. At the tip of a gall is a small opening ringed with Fig. 10. Black sage leaf galls induced by the sage leaf gall midge. tiny hairs.

3 Russo (1979) put it under Rabdophaga with the species name salviae, but it apparently is a name that is no longer used.

5 Fig. 11. More matured Black sage leaf galls induced by the sage leaf gall midge protruding from both sides of a leaf. They are about 2 mm long. Insert: closeup of dried galls.

On the black sage, the galls can also appear on the petiole instead of the leaves. On the leaves, they appear as reddish blisters (Fig. 10), but sometimes they can be green. The larger ones protrude from both sides of a leaf (Fig. 11). The gall remains round on one side of the leaf, while on the other side it develops into a characteristic urn with an opening ringed with hairs. These sage leaf galls are monothalamous. A point worth noting is that they look similar but not identical on the white and black sages. Different plants have different responses to the same chemicals secreted by a gall insect.

Willow Leaf Galls Similar to oaks, willows are attractive to many gall inducing insects. The easiest observable galls are the bean leaf galls, as shown here on Arroyo willow, Salix lasiolepis (Fig. 12).4 They are big and colorful. They are mostly red but sometimes can be green. These galls are induced by the willow leaf gall sawfly, Pontania pacifica. Sawflies are not flies. They are related to wasp (insect order Hymenoptera) in the common sawfly family, Tenthredinidae.5 They do not have the characteristic narrow “wasp waist.” The tenthredinids are called sawflies because of their sawlike ovipositors. What emerges from the gall is not the adult sawfly. After its last instar (insect

4 If you see not so pretty and smaller galls on willow leaves, they can be induced by a midge in the genus Lestodiplosis. Leaf rosettes are caused by the Willow Rosette gall midge (Rabdophaga salicisbrassicoides). Both are Cecidomyiids. 5 There is no trace to the meaning of the name. According to taxonomy record, it was chosen by the French zoologist Pierre André Latreille (1762–1833), also a renowned entomologist.

6 development stage), a larva molts into a prepupa, which escapes the gall and drops to the ground. It is on the ground among leaf litter that the prepupa makes the cocoon for the eventual pupation. These leaf galls are relatively large, over 10 mm in length, and protrude from both sides of a leaf (cannot be seen in Fig. 12). These galls are monothalamous, typically with one big larva (Fig. 12 insert). Nonetheless, one may find additional multiple escape pinholes. This is because plant galls are a biological community of its own that is inhabited by a variety of other insects (more in Part II).

Fig. 12. Leaf bean galls induced by a gall sawfly on Arroyo willow. Insert: A sawfly larva with plenty of frass (droppings).

Part II. Plant Galls

In this part, we cover some topics related to plant galls.

What triggers the gall formation? For as much as we know about the diversity of gall-inducing insects, we still have yet to have a good understanding of the stimuli that trigger gall formation. It would be logical to hypothesize that a female insect injects chemicals into a plant while it lays its eggs. Or after the eggs hatch, the larvae secrete chemicals. All these chemicals may be related to or function similarly as cytokinins and auxins—plant hormones that regulate cell division, enlargement, and tissue development. The nibbling of the larvae as they feed on plant tissue may also provide a mechanical stimulus to trigger the growth of a gall. And all these stimuli may play a role depending on the particular circumstance. For example, it has been suggested that the larvae of cynipid wasps are responsible for initiating gall development. This may explain the variation in the gall size. The female

7 wasp may lay just a few or many eggs. With tenthredinid wasps, galls often do not develop until the eggs hatch, but willow leaf galls can reach full size before the eggs hatch. While it appears that the egg-laying Pontania sawfly, a tenthredinid, is responsible for gall initiation, secretions from the larvae also help. Experiments using extracts from young Pontania larvae have been shown to promote the continued growth of galls. Furthermore, different alternating generations of an insect (see next section), especially with cynipid wasps, can cause different types of gall on different parts of the same host plant. There are simply too many variations in insect-plant host interactions that we cannot make any general statement on the mechanism of gall initiation.

Gall inducing insects have complex life cycles The gall inducing insects that we have covered here go through complete metamorphosis, but how they reproduce is a bit more complicated. Many species, most cynipid wasps and some gall midges, have alternating generations that reproduce differently (called heterogeny). One of the generations carries out sexual reproduction, but in the other, unfertilized eggs from the female can develop into sexual offspring. This phenomenon is called parthenogenesis.6 Many cynipid wasps undergo two different generations each year. Let’s say in the spring, a bisexual generation is spawned from the galls. They mate and initiate new galls. When these galls mature in late summer or early fall, only parthenogenetic females emerge. They overwinter in diapause (a dormant state), and next year lay eggs to initiate new galls which give rise to the bisexual generation. Depending on the species, the order of these two generations can be reversed. Again, each generation can induce different galls on different parts of the host plant. After saying all this, the California gall wasp (Andricus quercuscalifornicus), which induces the oak apple gall, is comprised of only parthenogenetic females even though they also make two rounds of galls each year. (There are no known males of this species.) On the other hand, the Pontania sawfly has only one generation a year even though its adults have short lives of a couple of weeks.

Plant galls are complex biological communities A plant gall is not only home to the gall-inducing insect, it is a food source that is very inviting to other insects. In a way they are parasites or predators to the gall-inducing insect by taking advantage of either the gall or the host insect. Some of them feed on the gall tissue; they are called inquilines. Others prey on the gall-inducing insect, but indirectly. The predators inject eggs into the gall near the host larvae, and it is the predator larvae that kill the host. Parasites that eventually kill their hosts are called parasitoids.

6 The root of parthenogenesis is from the Ancient Greek, parthénos, for a maiden or virgin, and génesis, for origin, generation or creation.

8 Furthermore, there are other parasitoids that prey on the inquilines and parasitoids; they are called hyperparasitoids. Thus the plant gall contains a complex biological community with a multi-trophic level food web. Outside of the insect world, woodpeckers are known to be gall-insect predators, especially on the large oak apple galls. When a gall falls to the ground, it is fair play for small animals like rodents. Some of the trophic interactions in an oak apple gall are shown in Fig. 13, taken from a study on Valley oak (Quercus lobata). The gall is induced by the California gall wasp (Andricus quercuscalifornicus). Its larvae are preyed upon by three parasitoid wasps. The most common is an Eulophid wasp (family Eulophidae), followed by an Eurytomid wasp (family Eurytomidae), and a Torymid wasp (family Torymidae) that is more common in smaller galls. This apple gall has two inquilines. The most common one is an anobiid beetle (a.k.a. furniture powderpost beetle, family Anobiidae), which feeds voraciously even on desiccated gall material. The other is a filbertworm moth (or just filbert moth, family Tortricidae), which itself is preyed upon by a parasitoid, a Braconid wasp (family Braconidae).

Fig. 13. Some of the most common interactions found in oak apple galls on the Valley oak from Joseph et al. (2011). See main text for the descriptions.

Wasps can make the most ghastly horror movies We know about how tarantula hawks (a spider wasp, Pompilidae) paralyze tarantulas such that their larvae can eat the prey live. They are not the only wasps that can be so gruesome. Pinhead-sized parasitoid wasps likewise victimize other gall wasps. Their larvae eat the larvae of their hosts inside out in a very organized way. They eat and torture their hosts until the time is right before killing them. A well studied parasitoid is the crypt-keeper wasp (Euderus set), which preys on at least seven different species of gall wasps. This crypt-keeper is one of the chalcid wasps

9 in the superfamily Chalcidoidea, a name that is taken from the Greek khalkos, meaning copper, for their metallic color. The species name set refers to Set (also Seth), the ancient Egyptian god of disorder and violence. A crypt is another name for a stem gall. One of the victims of the crypt-keeper is the cynipid wasp Bassettia pallida, which induces stem galls on oak trees in the Southeastern United States. As a gall wasp, the developed adult has to chew through the thick, woody gall wall to escape. For a gall that is parasitized by the crypt-keeper, the adult makes an unusually smaller hole, and they are dead, blocking the exit with their head. What happened? After a crypt-keeper injects her eggs into a gall, the hatched larvae start feeding on the gall wasp. The details here are unclear, but scientists have discovered crypt-keeper larvae and pupae in the adult bodies of the B. pallida when they perform autopsies. As soon as a B. pallida adult makes a small hole, the crypt-keeper larva stops it such that the B. pallida head plugs up the hole like a cork and remains unresponsive. After a few more days, a matured adult crypt-keeper eats through the B. pallida, crawls into and pops out through the head of the poor, dead host.

Oak galls can be used to make writing ink Historically, writing ink was carbon ink made from soot of burning oil or resin. Around several centuries into the Common Era (CE), carbon ink was replaced by iron gall ink (also called the oak gall ink or iron gall nut ink) in virtually all important documents. Two notable ones are Codex Sinaiticus, the first bible written on parchment in the 4th century, and the U.S. Constitution. Iron gall ink was used until it was replaced by synthetic pigments in the 20th century (but it is still sold for making art). So what is iron gall ink? The two key ingredients are tannic acid and iron sulfate (vitriol, its archaic name). And needless to say, the historic source of tannic acid is oak gall.7 These two chemical compounds can react to form a dark complex that penetrates parchment and paper, making it difficult to erase as writing ink. This is why iron gall ink was used in writing important documents. Nobody knows who invented the ink, but it is often mentioned that Pliny the Elder (23–79 CE) wrote briefly his observation that a leaf of papyrus turned black when it was steeped in an infusion of nut-galls.8 So long story short for a visitor: Do you know that for a good part of two thousand years, oak gall was used to make writing ink?

What is the difference between galls and witches’ broom? What is called witches’ broom is another deformed plant growth. It can be caused by insects, mites, nematodes, fungi, bacteria and virus, and in older literature it is often

7 Oak gall contains gallotannic acid, which is slightly different from quercitannic acid found on oak bark and leaves. Both are complex, polyphenolic compounds. Since the early days, tannic acid from other plants could also be used in making ink. 8 That is in his Naturalis Historia, Book 34, Chapter 26.

10 being discussed together with galls. Also, dwarf mistletoe (Arceuthobiurn campylopodum) can parasitize conifers in the Southwestern United States, and some of them can further induce a tree to make witches’ brooms. Some of the earliest observations of witches’ broom were caused by rust fungi,9 to the extent that some were called witches’ broom galls. Our current perception of witches’ brooms is that they are mostly a dense cluster of stems or branches growing from a focal point on a tree. Thus the form is largely globular. The primary agents are virus and phytoplasma that can change the pattern of gene expression in the host plant cells. The resulting deformed growth lasts a long time, typically the remaining life of the host plant. Insects, if they appear to be an agent, would rather be vectors or carriers of these microorganisms. Phytoplasma, briefly, is a tiny, primitive bacterial cell that has to live within a host cell like a virus.10 This microorganism was discovered in 1967, a while back but still long after much of the classical studies of witches’ broom. Being primary agents does not mean exclusive, and here are some examples of fungi and bacteria. The fungus Taphrina betulina is what causes birch and cherry trees to make witches broom, the kind of dense clusters similar to what we see on Torrey pines. Some bacteria are capable of altering the gene expression of a host cell. These bacteria carry a tumor-inducing (Ti) plasmid, an extranuclear chromosome, that is transferred into the plant tissue, and some genes on the plasmid can be integrated into the plant cell genome. One example is the bacterium Agrobacterium tumefaciens which causes root crown galls in a good number of plants. Another bacterium that carries a Ti plasmid is Rhodococcus fascians, and the herbaceous plants infected by it make leaf deformations called either witches broom or leaf gall, depending on the particular plant. Hence, when in doubt, let it be; it is not always easy to tell whether a malformation should be called a witches’ broom or a gall.

9 Rust fungi are called as such because they generally make reddish brown freckles on infected plants, but when it invades the stem, it can stimulate the development of shoots. Rust fungi require living hosts as a source of nutrients, and their hyphae can grow into a host plant cell. 10 More details. Phytoplasmas have a cell membrane but no cell wall, and they have also lost most metabolic genes and are highly dependent on the host cell for metabolism. Their genome is roughly one-fifth the size of a typical bacterium like E. coli. Other than causing witches’ broom, which is the proliferation of shoots, phytoplasma can cause a wide range of symptoms on many plants, including stunting, yellowing, and formation of leaf-like tissues instead of flowers (phyllody). Phytoplasmas are transmitted by insect vectors.

11 Part III. Witches’ Broom

This final part looks into the witches’ brooms that we see on a few pines in TPSNR, but nonetheless pique the curiosity of many visitors. Quick response to a visitor: The abnormal growth that we see is called a witches’ broom, and can happen to other trees elsewhere. It can be caused by some kind of pathogen, in which case a good analogy is that it is like a skin wart. Or it can be due to cell mutation in a growing stem, which may be the case here. Either way, the abnormality looks odd but it won’t kill the tree. The long answer follows.

Where is the broom in the witches’ broom? A dense round cluster of stem or branches does not resemble a broom. The term came from observations of deformed plant growths that resemble an old-fashioned straw broom. Fig. 14 is a classic photo plate of a witches’ broom from the highbush blueberry (Vaccinium corymbosum). This witches’ broom is caused by the rust fungus Pucciniastrum goeppertianum, which can also infect conifers. And how did the witch come into the picture? Mushrooms, or fungi, and related anomalous plant growths were steeped in folklore and superstitions in medieval Europe.11 The term “witches’ broom” came from the German word Hexenbesen, which combines to bewitch (hex) and a bundle of Fig 14. A witches’ broom from a highbush twigs (besom). The real reason is long lost. blueberry taken from Fordham (1967). One belief was that the growth was caused by the flight of witches over the affected trees at night, and this would provide plentiful supply of brooms for future flights. Back then, witches were also held responsible for the blight of crops (fungal infections that cause plants to have blotches or blights).

Witches’ broom on pines in Eastern Europe There were few academic studies of witches’ broom on conifers, with the exception of the Siberian stone pine (Pinus sibirica). The results identify two primary causes of witches’ broom on this pine. One is infection by phytoplasma. (But with other plants, one

11 We may recall how mushrooms are key ingredients used by witches for potions. Some of the strongest ties between fungi and witches are in Russian folktales about the witch Baba Yaga.

12 still cannot rule out rust fungus or virus.12) The other is cell mutation in the growing tip (or bud) of a shoot that leads to excessive branching.13 These results may shed some light on what is observed at TPSNR. The witches’ brooms on the Siberian pine that arise from cell mutation at a stem tip are dense and compact. This is due to increase branching of smaller or slower growing shoots. The shoots retain the capability to make seed cones, even though they are smaller than usual. There are no pollen cones. These brooms have normal longevity, and can be used to make dwarf ornamental plants. In contrast, the witches’ brooms caused by a pathogen tend to be small and scattered at different locations, and each one has a noticeable focal point of growth. They do not make cones, have a sickly appearance, and do not last long.

Torrey pine witches’ broom Now that we know a bit more about witches’ brooms in general, we can elaborate the ones found in TPSNR with a few more comments. To begin, we may want to take note that in all incidences, there is only one witches’ broom on a given tree. Of the thousands of Torrey pines, there are only a handful of trees with a witches’ broom, and these trees are spaced far apart from one another. These are not patterns of infection by pathogens that are dispersed by wind or insect vectors. With the particular pine near Razor Point where the Weeders can take a close look (Fig. 15), the witches’ broom is an extremely dense outgrowth consisting of many branches. The needles are relatively short for a Torrey pine, and there is a higher variability of the number of needles in a cluster. Especially sampling father into the broom, there are more clusters with only four needles.14 However, unlike the normal branches on the tree, there are no seed cones in the witches’ broom.

12 As in scientific literature, we include virus even though there are only a handful of cases where a virus is clearly identified. The most notable ones are a potato disease, and the cause of rose rosette by a virus spread by a mite. With conifers, virus appeared only in very old papers, and one can trace the gradual change to phytoplasma in the years after it was discovered. 13 More precisely, the cell mutation is somatic mutation in the stem apical meristem. Meristem is undeveloped plant tissue that can grow into other kinds of cells and structures. They are equivalent to stem cells in animals. Meristem can be found in the tips of a root and a growing shoot, hence the adjective apical. Somatic mutation occurs in a typical cell and is not hereditary, unlike germline mutation in a seed or a pollen. 14 The needle number counting is from Carson (1999). In general, variability of the number of needles in a cluster is an evolutionary adaptation of pines. The number drops below average when there is a large moisture deficit.

13 Fig. 15. The Torrey pine near Razor Point with a witches’ broom.

With all the information at hand, and compared with the Siberian stone pine, the witches’ broom in Fig. 15 fits the description of one due to cell mutation, but with one exception—that it has no seed cones. Or no longer has the cones.15 Even without seed cones, cell mutation being responsible for the abnormal growth is still highly probable with what we have in TPSNR. However, given the fact that we have yet to analyze the genetics of the witches’ broom, saying that we are not absolutely certain of the cause of the witches’ brooms in TPSNR would still be an acceptable answer.

Annotated Bibliography ● To find gall insects images

BugGuide, hosted by Iowa State University Dept of Entomology. Available from https://bugguide.net/ – To find the images of a specific insect, copy and paste the scientific name of the insect into the search box. To do a general search, just enter, say, “oak galls” into the search box.

Natural History of Orange County compiled by Peter J. Bryant at U.C. Irvine, including a collection of arthropods; available from http://nathistoc.bio.uci.edu/Arthropods.htm – Like all crowd-source media, BugGuide is not always reliable. The collection curated by Bryant himself is a lot smaller but extremely well done and trustworthy.

● Related to plant galls

(2008) Gall. In: Capinera J.L. (ed) Encyclopedia of Entomology. Springer, Dordrecht. Available

15 From an extended abstract of a research paper which is not accessible, cones are found when the witches’ broom is at the top of the tree crown. Carson (1994) wrote that “Torrey broom seeds” were collected at the tree in Fig. 15. Back so many years ago, the broom might have been in the tree crown.

14 from https://link.springer.com/referenceworkentry/10.1007/978-1-4020-6359-6_1021 – Just brief descriptions, but has good references. Take note of the navigation bar on the left. There are more specific entries for the key gall inducing insects.

Caltagirone, L.E. (1964). Notes on the Biology, Parasites, and Inquilines of Pontania pacifica (Hymenoptera: Tenthredinidae), a Leaf-Gall Incitant on Salix lasiolepis. Annals of the Entomological Society of America 57, 279–291. – A very old paper but extremely thorough study of the gall sawfly and also the inquilines and parasitoids that live in a willow leaf gall.

Joseph, M.B., Gentles, M., and Pearse, I.S. (2011). The parasitoid community of Andricus quercuscalifornicus and its association with gall size, phenology, and location. Biodiversity and Conservation 20, 203–216. – A detailed study of the community of parasitoids and inquilines in cynipid-induced galls on the California valley oak.

Russo, Ronald A. (1979). Plant Galls of the California Region, Boxwood Press. – An old but still very informative little book. The Docent Library has a copy. Russo has a newer book in 2007, Field Guide to Plant Galls of California and Other Western States.

Swiecki, T.J. & Bernhardt, E.A. (2006). A Field Guide to Insects and Diseases of California Oaks (Report PSW-GTR-197). Retrieved from Forest Service, USDA: https://doi.org/10.2737/PSW- GTR-197 – Has a section on gall wasps and the erineum mite.

Ward, Anna K. G., Khodor, O.S., Egan, S.P., Weinersmith, K.L., and Forbes, A.A. (2019). A keeper of many crypts: a behaviour-manipulating parasite attacks a taxonomically diverse array of oak gall wasp species. Biology Letters 15, 20190428. – A follow up study of Euderus set by the group of Forbes and Egan.

Weinersmith, K.L., Liu, S.M., Forbes, A.A., and Egan, S.P. (2017). Tales from the crypt: a parasitoid manipulates the behaviour of its parasite host. Proceedings of the Royal Society. B: Biological Sciences 284: 20162365. – The first reported study of the parasitoid Euderus set.

● Related to witches’ broom. Most of the studies on the Siberian stone pine were carried by scientists at the Russian Academy of Sciences.

Carson, John (January 1999). Torrey Witches’ Brooms – A Little More Data, A Lot More Questions, Torreyana, Torrey Pines Docent Society. – A follow up to his 1994 article. Mentioned that a high school student had counted the needles in the witches’ broom and found a high variability, but then he also found that the trees near the Lodge also had some variability in the needle numbers.

Carson, John (May 1994). Witches’ Brooms, Torreyana, Torrey Pines Docent Society. – A column in which Carson explained why he believed cell mutation is the cause of the witches’ broom in the Reserve. He wrote that Hank Nicol had collected some “Torrey broom seeds,” and so long ago, the witches’ broom might very well be in the tree crown and could bear seed cones. Moreover, the growth of the germinated seeds was normal, suggesting that there was no pathogen, and if there was mutation in the broom, it was not hereditary.

15 Dugan, Frank M. (August 2008). Fungi, Folkways and Fairy Tales: Mushrooms & Mildews in Stories, Remedies & Rituals, from Oberon to the Internet, North American Fungi 3, 23-72. – A paper on the relation between fungi and witch folklore, but provided a lead to Rolfe & Rolfe (1925) on witches’ broom.

Fordham, Alfred J. (June 23, 1967). Dwarf Conifers From Witches'-Brooms, Arnoldia 27, 29-50. – An old paper that provides some historical perspective of witches’ brooms.

Hogenhout, S.A., Oshima, K., Ammar, E., Kakizawa, S. Kingdom, H.N., and Namba S. (2008). Phytoplasmas: bacteria that manipulate plants and insects. Molecular Plant Pathology 9, 403–423. – A review on phytoplasmas.

MacLean, A.M., Orlovskis, Z., Kowitwanich, K., Zdziarska, A.M., Angenent, G.C., Immink, R.G.H., and Hogenhout, S.A. (2014). Phytoplasma Effector SAP54 Hijacks Plant Reproduction by Degrading MADS-box Proteins and Promotes Insect Colonization in a RAD23-Dependent Manner. PLOS Biology 12: e1001835. – Work from the group of Saskia Hogenhout, discovering a probable molecular mechanism of phytoplasmas. The phytoplasma in this work makes a protein that interferes with a family of transcription factors that regulates tissue development.

Mathiasen, R.L. (2019). Susceptibility of Coulter pine (Pinus coulteri) to western dwarf mistletoe (Arceuthobium campylopodum) in southern California. Forest Pathology, article: e12543, early preview edition. – Unlike relatively benign witches’ broom caused by microorganisms, dwarf mistletoe can severely impact the health of the conifer and increase mortality.

Rolfe, R.T., and Rolfe, F.W. (1925). The romance of the fungus world. An Account of Fungus Life in its numerous guises, both real and legendary, Chapman and Hall Ltd., London. (Google uses a 1974 reprint from Dover Publications, New York.) – Has a chapter on witches’ broom and mentioned the flight of the witches. This very old book has a digitized edition available on Google Books.

Śliwa, H., Kaminska, M., Korszun, S., and Adler, P. (2008). Detection of ‘Candidatus Phytoplasma pini’ in Pinus sylvestris trees in Poland. Journal of Phytopathology 156, 88–92. – A study of the witches’ broom on Siberian stone pine. Making use of molecular biology techniques, this group identified the DNA of phytoplasma ribosomal RNA, meaning that this microorganism is responsible for the formation of witches’ broom in this study location.

Vasilyeva, G., and Zhuk, E. (2016). Needle structure of mutational witches’ brooms in Pinus sibirica, Dendrobiology 75, 79–85. – A study of the Siberian stone pine. The key is that the needles from the mutational witches’ broom are shorter and thinner.

Yamburov, M.S. & Goroshkevich, S.N. (2008). Witches' brooms in Siberian stone pine as somatic mutations and initial genetic material for breeding of nut-bearing and ornamental cultivars, Ann. For. Res. 51: 165-166. – An extended abstract on a study of the Siberian stone pine. Mentioned that with cell mutation, there were no male cones, and female cone initiation was normal only if the witches’ broom was (still) located in the top part of a crown.

Zhuk, E., Vasilyeva, G. and Goroshkevich, S. (2015). Witches’ broom and normal crown clones

16 from the same trees of Pinus sibirica: a comparative morphological study. Trees 29, 1079–1090. – A study of the Siberian stone pine. The extent of the expression of cell mutation governs the variability of the morphology of the witches’ broom.

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