Our knowledge of the biology of Siricidae is uneven. We know very little about most genera and species except for Sirex noctilio, which, as the major pest of pines in the Southern Hemisphere, was the focus of an intense and successful classical biological control program in the 1960s, 70s and 80s (Haugen and Underdown 1990, Haugen et al. 1990). Much of what we know about the biology of S. noctilio has been summarized in review papers by Morgan (1968) and Talbot (1977) and most recently in several chapters of the book The Sirex Woodwasp and its Fungal Symbiont (Slippers et al. 2011). We do not attempt to match the details of these works here but instead present a generalized version of siricid biology, leaning heavily on our knowledge of S. noctilio. Although we use it as our model species, it is important to recognize that S. noctilio differs fundamentally from most other species in that, where it is adventive, it attacks and kills stressed but relatively healthy trees. In its native range, like most other siricids, it is relatively benign.
The central paradigm of siricid woodwasp biology is that they live in symbiotic relationships with basidiomycete wood decay fungi (Buchner 1928, Cartwright 1929, 1938, Clark 1933, Francke-Grossman 1939, Stillwell 1960, 1962, 1964, 1965, 1966, 1967 and Gaut 1969, 1970, Slippers et al. 2003, among others). Female woodwasps carry fungal arthrospores, oidia or hyphal fragments in paired abdominal glands (intersegmental pouches) called mycangia and inoculate their tree host with fungus at oviposition. The fungus grows through the tree and larvae feed on the fungus as they bore through the wood. This relationship is mutualistic and obligate as far as we know for all genera and species except the genus Xeris. Adult females of Xeris species have significantly reduced glands that do not contain a wood decay fungus. They oviposit exclusively into trees that have already been attacked by another genus of woodwasp and infested with an appropriate wood decay fungus (Franke-Grossman 1939, Stillwell 1966, Spradberry 1976, Fukuda and Hijii 1997).
Early literature attempting to associate siricid species with specific symbionts was confusing because it was difficult to identify the fungi using classical methods and the Siricidae were in need of revision (Morgan 1968, Talbot 1977). With the development of molecular identification methods and taxonomic revisions, associating each siricid woodwasp with its specific symbiont has become less problematic. To date, four species of basidiomycete wood decay fungi are associated with Siricidae. Tremex columba (Stillwell 1964), T. fuscicornis in Poland (Pažoutová and Šrǔtka 2007), T. longicollis in Japan (Tabata and Abe 1995), and Eriotremex formosanus (Schiff unpublished data from North America) use Cerrena unicolor whereas Sirex noctilio, S. nitobei from Asia and S. juvencus from Europe use Amylostereum areolatum (Gaut 1969, 1970); Urocerus japonicus and U. antennatus both from Japan use Amylostereum laevigatum (Tabata and Abe 1997, 1999) and all other siricids examined (including Sirex cyaneus, S. imperialis, S. areolatus, S. californicus, S. nigricornis, S. varipes, Urocerus californicus, U. flavicornis, U. gigas, U. augur and U. sah (Stillwell 1966, Gaut 1970, Schiff unpublished data) use Amylostereum chailletii. Although woodwasp/fungus specificity is generally accepted, a recent exception was the isolation of Amylostereum areolatum from two specimens of Sirex nigricornis (formerly edwardsii) that were reared from logs also infested with S. noctilio. Presumably, the S. nigricornis acquired A. areolatum when they fed on parts of the tree already infested by the symbiont from S. noctilio (Nielsen et al. 2009).
In the Sirex noctilio /Pinus radiata association, the symbiotic fungus has two basic functions; it provides food for developing woodwasp larvae and, in conjunction with phytotoxic mucus, it kills the tree, rendering it more suitable for fungal growth. Like most wood boring insects, siricids do not make the complex of cellulases necessary to digest wood and must either obtain them from symbionts or eat something that digests cellulose for them (Chapman 1982), in this case the symbiont itself (mycophagy). Indirect evidence suggests they do both. Sirex cyaneus larvae have been observed to live and grow for three months on pure culture of their symbiont (Cartwright 1929) and Kukor and Martin (1983) demonstrated that S. cyaneus acquired digestive enzymes from its fungal symbiont, Amylostereum chailletii. Fungal mediated nutrition is very important to Sirex noctilio and fungal growth is positively correlated with adult size and thus fecundity, and dispersal ability (Madden 1981).
The ability to kill the host tree with fungus and mucus distinguishes Sirex noctilio from most other siricids and is the reason why S. noctilio is a major pest of some hosts whereas most other woodwasps are not. Oviposition behavior of S. noctilio has been well studied. Females drill into stressed trees and depending on the tree’s response either deposit eggs followed by a dose of fungus and mucus in a separate shaft (Coutts and Dolezal 1969, Madden 1981), or they deposit only the fungus and mucus. In the latter case, injecting only fungus and mucus is adaptive because the tree is rendered more suitable for future oviposition. There are generic level differences in drilling behavior. Sirex species make from 1–4 drills per insertion of the ovipositor through the bark, only some of which contain eggs and/or fungus; Urocerus species make a single long drill with many eggs alternating with masses of fungus; Xeris species make from 1–5 long drills per insertion with a few eggs in each drill but no fungus (Spradbery 1977) and Tremex columba either leaves unfertilized eggs in the adult female emergence tunnel or up to 7 presumably fertilized eggs in each oviposition tunnel (Stillwell 1967). Siricids like other Hymenoptera are haplodiploid with unfertilized eggs becoming males and fertilized eggs developing into females. It is important to note that neither fungus nor mucus alone kills the tree — only in combination are they toxic (Coutts 1969a and b). The mucus, produced by glands in the female abdomen and stored in a median reservoir, weakens the tree’s immune response allowing the phytotoxic fungus to kill the tree. Woodwasps other than Sirex noctilio all have mycangia and mucus reservoirs but their function has not been well studied. Spradberry (1973) determined the effects of various combinations of mucus and fungus from three genera of woodwasps, Sirex, Urocerus and Xeris, on live trees or fresh branches of several coniferous hosts and found that Amylostereum areolatum and the mucus from Sirex noctilio on Pinus radiata was the most phytotoxic combination. This explains why S. noctilio has been such a great pest of P. radiata plantations in the Southern Hemisphere but does not explain the presence of mucus glands in non toxic species. Presumably, in other woodwasps the mucus helps condition the tree in a more subtle way to improve growth of the fungus. Recently, Tremex fuscicornis, adventive in Chile, has been reported to kill weakened hardwoods and even vigorous Acer negundo and Populus sp. (Baldini 2002, Ciesla 2003). Presumably, the combination of fungus and mucus from Tremex fuscicornis can kill selected hardwoods just as Sirex noctilio kills some pines. Perhaps comprehensive studies of the effects of fungus and mucus from different siricid species on a wide variety of exotic hosts may predict which species will become pests in adventive situations.
Adult behavior of Siricidae is poorly known except for Sirex noctilio. In general, males emerge from the tree earlier than females and fly to the tops of trees to form swarms (Madden 1982, Schiff unpublished data). Individual females are mated when they fly into the swarm; they then proceed to oviposit in weakened trees. Studies of S. noctilio indicate that females select the height of oviposition sites based on moisture content (Coutts and Dolezal 1965) and localized turgor pressure within the host (Madden 1968, 1981). Western North American Sirex and Urocerus species have been observed ovipositing in the base of burned trees where presumably the turgor pressure and moisture content are appropriate (Schiff unpublished data). At least in Sirex noctilio (Madden 1981), and presumably in other species, there is selection for host condition that is most favorable for growth of the fungal symbiont.
The life cycle of siricid woodwasps is quite varied. Some species develop in a single year others may take 2–3 years (Stillwell 1966, 1967) and some like Sirex noctilio and Tremex columba can rush part of the population through in less than one year while other individuals take a full year or more. Depending on the availability and quality of the fungus, there are from 6–12 larval instars (Stillwell 1928, 1967, Madden 1981) that can mine 5–20 cm for Sirex and Urocerus spp. and up to 3 m for Tremex columba up and down in the trunk of the host (Solomon 1995). Larvae are cylindrical and have a characteristic “S” shape with a cornus (spike) on the last segment. The cornus is thought to help the larvae pack the frass in the tunnel. When the larvae finish feeding they turn sharply to the outside of the tree leaving a characteristic “J” shaped end of the mine. As the exit mines are perpendicular to the surface of the tree, emergence holes are perfectly round. Female woodwasp larvae have paired hypopleural organs in the fold between the first and second abdominal segments (Parkin 1941, 1942, Stillwell 1965). These organs are believed to be involved with transfer of the symbiont to the adult (see Morgan 1968 and Talbot 1977 for discussion).
Most of our knowledge of the natural enemies of siricids comes from efforts to control Sirex noctilio in Australia. The primary effort was to search for natural enemies that controlled siricids in their native lands and determine if they could be used to control populations of S. noctilio adventive in Australia. Starting in the early 1960s a massive effort was made to search for and rear parasitic wasps (parasitoids of each siricid species are listed in a separate section of this publication). Many species were collected, reared, released and became established in Australia (Kirk 1974 and 1975, Spradberry and Kirk 1978, Taylor 1967a and 1967b and others) but the parasitoid wasp complex (including ichneumonids, ibaliids and stephanids) seldom killed more than 40% of the Sirex noctilio population and was not effective in preventing population outbreaks (Haugen et al. 1990). However, in 1962 nematode parasites were discovered in S. noctilio in New Zealand (Zondag 1962) and their biology was described a few years later (Bedding 1967, modified in 1972). The biology of the nematodes is intimately entwined with the biology of siricids and their fungal symbionts and is summarized briefly here. The nematode Beddingia (Deladenus) siricidicola has two alternate life cycles each with a different female morphology. The two forms, one mycetophagous and the other parasitic on siricids, are morphologically distinct and were originally thought to be representatives of two different nematode families, Neotylenchidae and Allantonematidae, respectively. The mycetophagous form feeds on fungal mycelium and will feed continuously for many generations as long as the fungus quality is maintained. If environmental conditions change or the nematode encounters a siricid larva, the alternate cycle begins. Juvenile nematodes develop into the alternate (parasitic) morphology and penetrate the cuticle of the siricid larva leaving a small dark mark at the entry site. In the haemocoel of the siricid larva, the nematode increases greatly in size, waiting to reproduce ovoviviparously when the woodwasp pupates. At the end of pupation juvenile nematodes emerge from their mother and migrate to the gonads of the adult woodwasp where they begin to feed on the eggs in the female or the testes in the male, respectively. The nematodes do not appear to affect the development or behavior of the adult wasp and when the female woodwasp emerges from the host she mates and oviposits in new trees. However, instead of depositing a new generation of woodwasps she deposits eggs filled with parasitic nematodes. As many woodwasps often oviposit into a single tree, the nematodes are quickly spread through the population, effecting control in as little as three years (Haugen and Underdown 1990). Male woodwasps infested with nematodes mate but do not transfer nematodes to females and are thus a dead end for the nematode. The use of nematodes to control woodwasps has been improved by development of techniques to handle nematodes and by selection of optimal strains (Bedding and Akhurst 1974, Bedding and Iede 2005, Bedding 2009). Seven species of nematodes parasitic on 31 host species (siricids or their parasitoids) have been described from around the world (Bedding and Akhurst 1978) and there are more awaiting description (Bedding, personal communication, Schiff, unpublished data). They can be divided into three groups based on their fungal associations. The mycetophagous form of Beddingia siricidicola feeds only on Amylostereum areolatum. The mycetophagous form of Beddingia rudyi, B. imperialis, B. nevexii, B. canii, B. proximus and an undescribed species feed only on Amylostereum chailletii and the mycetophagous form of Beddingia wilsoni feeds on both. Even though they do not carry a fungal symbiont of their own, Xeris species, like many of the wasps parasitic on siricids, can be parasitized by Beddingia species (Bedding and Ackhurst 1978, see table 2). This information is presented in a table in Bedding and Akhurst (1978) with the siricid hosts. Taxonomic revisions of the Siricidae and easier methods to identify fungal symbionts may change this information slightly; for example, Urocerus japonicus and U. antennatus are listed as using Amylostereum chailletii instead of A. laevigatum as their symbiont.
Although they cannot be easily manipulated to target a particular infestation, birds are also natural enemies of both adult and larval siricids. In Tasmania, the dusky wood swallow, the forest raven, and the spine-tailed swift, attacked mating swarms of Sirex noctilio in the tops of trees to such an extent that they altered sex ratios in the next year’s population (Madden 1982), and Spradberry (1990) found an overall larval predation rate of 28.8% by woodpeckers in a European study.
