Ceracis californicus, (CASEY)

Madenjian, James J., Regensberg, Pamela & Caterino, Michael, 2016, Ceracis californicus (Casey) (Coleoptera: Ciidae): Newly Recognized Herbarium Pest, The Coleopterists Bulletin 70 (1), pp. 137-141 : 137-141

CERACIS CALIFORNICUS (CASEY) ( COLEOPTERA : CIIDAE ): NEWLY RECOGNIZED HERBARIUM PEST

JAMES J. MADENJIAN U. S. Food & Drug Administration 19701 Fairchild Irvine, CA 92612, U.S.A.

PAMELA REGENSBERG Denver Botanic Gardens 909 York Street Denver, CO 80206, U.S.A.

AND

MICHAEL CATERINO E-143 Poole Agricultural Center Clemson University Clemson, SC 29634, U.S.A.

Ceracis californicus (Casey) is a minute tree fungus beetle ( Ciidae ). Larvae and adults of the family bore into and feed upon sterile hyphae, which comprise the bulk of the fruiting structures (sporophores = mushrooms) of Polyporaceae and other Basidiomycota that grow on woody structures ( Lawrence 1974). Ciid densities can be very high (1,000 or more individuals per sporophore) ( Graves 1960). Ciids are mycetobionts, spending most of their lives within the sporophores and being entirely dependent on them for food and shelter ( Lawrence 1973). This is consistent with Graves ’ (1960) speculation that some individuals may live their lives in one sporophore.

Ciid adults can be recognized by the following characteristics ( Lawrence 1971): (1) head usually declined and partly concealed by the pronotum; (2) eyes oval and entire; (3) frontoclypeal area in male often raised to form a ridge, tubercles, or horns; (4) antennae 8- to 10-segmented with a 2- or 3-segmented club bearing large, complex sensilla; (5) anterior edge of pronotum in male often bearing tubercles or horns; (6) tarsal formula 4-4- 4 in both sexes, the tarsal segments simple (not lobed beneath); (7) abdomen with five freely articulated sternites.

During 2010, Pamela Regensberg (Curatorial Assistant) discovered a live ciid infestation of sporophores in the Sam Mitchel Herbarium of Fungi, Denver Botanic Gardens, Denver, CO. Ciids were found in Cabinets 12, 13, and 14 (containing the herbarium ’ s entire collection of the Order Aphyllophorales ). Sporophores from Cabinet 13 were the most heavily infested. These specimens — housed in telescoping boxes of various sizes — and specimens from a nearby display shelf were placed in a residential, upright freezer for a minimum of two weeks during 2010. The cabinet was sanitized before specimens were returned to the collection. The herbarium obtained a − 20°C chest freezer in February 2011, and staff began refreezing specimens from Cabinet 13 to ensure beetle mortality. Specimens in Cabinets 12 and 14 were subsequently placed in the freezer for a minimum of 14 days. Each cabinet was sanitized before specimens were returned. The entire process took several months and was completed during the summer of 2011. Prior to the freezer treatments, Pamela collected 37 samples of beetles / frass / fungal fragments from infested specimens representing 22 or 23 different species of fungi. Individual samples were carefully collected and placed in acid-free envelopes labeled with the taxon name and the herbarium accession number. She observed beetles living and breeding (as evidenced by tunneling, fragmentation, and frass) in these herbarium specimens.

The samples were sent to James Madenjian at the US Food & Drug Administration in Irvine, CA. Most of the samples were simply examined microscopically (Wild M5A dissecting microscope). A wet extraction method (AOAC (18 th Edition) 967.24B) ( Ziobro 2005) was used for seven of the samples with large fungal fragments. Whole and equivalent to whole (heads counted) ciid larvae, pupae, and adults were counted. The search for larvae, particularly smaller ones, was not thorough for some samples. All of the ciid adults were identified (with the aid of a Leica M165 FC microscope) as C. californicus .

Twenty point-mounted voucher specimens (from 18 different species of fungi) were sent to Michael Caterino for identity confirmation and deposition in the Santa Barbara Museum of Natural History; Santa Barbara, CA. Twenty-eight other pointmounted voucher specimens (from 20 different species of fungi) were deposited in the reference collection of the Pacific Regional Laboratory Southwest Microanalytical Section, US Food & Drug Administration, Irvine, CA.

The 23 fungal taxa are presented in alphabetical order with the mean number of C. californicus adults per sample ( Table 1). The means ranged from 1 to 612. Nomenclature follows Index Fungorum (www.indexfungorum.org).

This study documents the herbarium pest status of C. californicus . No previous literature on this specific subject was found. The damage to some of the attacked herbarium specimens was so severe ( Fig. 1 ) that the specimens were de-accessioned and discarded.

As a result of this infestation, preventive measures and strict sanitation protocols were instituted. Members of the herbarium staff assumed that the infestation originated from incoming infested specimen(s). Now, before any fungus belonging to the Aphyllophorales is accessioned, the speci- men must be thoroughly dried, preferably off-site, and then placed in a − 20°C freezer for a minimum of 14 days. Cabinets 12, 13, and 14 must be thoroughly inspected at least once per month. To ensure that new outbreaks are immediately detected, herbarium staff individually removed every specimen from its box and discarded any loose material — dead beetles, frass, or other debris.

Several species of ciids are recognized as pests. Hagstrum and Subramanyam (2009) listed the following six species as pests of commercial food / herbal medicine: Cis asiaticus Lawrence , Cis chinensis Lawrence , Cis mikagensis Nobuchi and Wada , Cis multidentatus (Pic) , Cis pygmaeus (Marsham) , and Orthocis auriculariae Lawrence. However, Lopes-Andrade (2008) suspected that C. chinensis , C. mikagensis , and C. multidentatus may actually represent only one species. Additionally, Linghua et al. (1994) listed Octotemnus parvulus Matsuo Miyatake and a species of Ennearthron Mellié as stored-product pests in China and Japan. Jian et al. (1999) reported a species of Plesiocis Casey as a pest of the commercial mushroom Ganoderma lucidum (Curtis) P. Karst. Only one ciid species, Hadraule blaisdelli (Casey) , has been recognized as a pest of sporophores in herbaria ( Lawrence 1971).

Ceracis californicus is found in western North America from Seattle, Washington east to western Nebraska, south along the Pacific coast to southern California and through the Great Basin and Rocky Mountain regions to southern Arizona and New Mexico; extending into Mexico as far as Baja California Sur and southern Sinaloa ( Lawrence 1973, 1974). Its geographic range includes a portion of Colorado including Denver ( Lawrence 1967). C eracis californicus is the only species in the genus that has been found in Colorado.

Hadraule blaisdelli is also found in western North America, from southern British Columbia to southern California, east through Utah, Arizona, and New Mexico into Texas and south into Mexico ( Lawrence 1973). It has also been found in Michigan, Iowa, Connecticut, Massachusetts, and Florida, but all of these records with the exception of Michigan represent herbarium infestations.

Differentiating adult features between C. californicus and H. blaisdelli include the following: (1) former with 3-segmented antennal club and latter with apparently a 2-segmented antennal club ( Lawrence 1974); (2) former with shorter prosternum in front of coxae (only slightly longer than intercoxal process) and latter with longer prosternum in front of coxae (twice as long as intercoxal process) (Thayer and Lawrence 2002); (3) males of former with pronotal horns and males of latter without pronotal horns ( Lawrence 1967; Klopfenstein 1971).

Ceracis californicus is a polyphagous species. Lawrence (1967, 1973, 1974) listed 15 breeding host species and five other host species. Our study substantially broadened the host list, at least as to the sporophores that may be consumed in museum situations. Seventeen species of infested fungal specimens represented new host records ( Table 1).

Members of the herbarium staff noted that specimens of the following genera exhibited the most damage: Bjerkandera P. Karst. , Cryptoporus (Peck) Shear , Fomes (Fr.) Fr. , Fomitopsis P. Karst. , Ganoderma P. Karst. , Gloeophyllum P. Karst. , Inonotus P. Karst. , Phellinus Quél. , Polyporus P. Micheli ex Adans. , Trametes Fr. , and Trichaptum Murrill. In contrast, specimens of some genera were situated in the three infested cabinets, but were undamaged. These genera included Daedalea Pers. , Daedaleopsis J. Schröt. , Favolus Fr. , Laetiporus Murrill , Oligoporus Bref. , and Pycnoporellus Murrill.

Different ciid species have different host preferences, and the beetle species can be grouped based on these fungal host preferences. Genera of fungi can be linked to these groups. Orledge and Reynolds (2005) used cluster analysis to establish six host-use groups among ciids, and they placed C. californicus in the Ganoderma ciid host-use group. The fungal hosts attacked by C. californicus in the herbarium ( Table 1) are linked not only to the Ganoderma ciid host-use group, but also to the Trametes , Phellinus , and Trichaptum ciid hostuse groups.

Ceracis californicus certainly appears to have the capacity to become a commercial mushroom pest. One of the attacked fungal species in the herbarium, Polyporus tsugae (Murrill) Overh. , is a commercial species (Chang and Miles 2004). Three of the host species listed by Lawrence (1967, 1973, 1974), G. lucidum , Ganoderma applanatum (Pers.) Pat. , and Pleurotus ostreatus (Jacq.) P. Kumm. , are also commercial mushroom species (Chang and Miles 2004). China, Korea, and Japan are the main producers and suppliers of the medicinal mushrooms of G. lucidum , G. applanatum , and P. tsugae (Chang and Miles 2004) .

Figures

Fig. 1. Damaged and de-accessioned specimen DBG23883, a sporophore of Gloeophyllum abietinum (Bull.) P. Karst.