Bry. Div. Evo.

40 (0): 001–005 ISSN 2381-9677 (print edition)

http://www.mapress.com/j/bde BRYOPHYTE DIVERSITY &

Copyright © 2018 Magnolia Press Article EVOLUTION

ISSN 2381-9685 (online edition)

https://doi.org/10.11646/bde.40.1.1

The first insect-induced galls in bryophytes

TAKAYUKI OHGUE1,3, YUME IMADA1, AKIRA ARMANDO WONG SATO1, JUANA ROSA LLACSAHUANGA
SALAZAR2 & MAKOTO KATO1
1
Graduate school of Human and Environmental Studies, Kyoto University, Yoshida-nihonmatsu-cho, Sakyo-ku, Kyoto, 606-8501, Japan
2
Centro de Datos para la Conservación, Universidad Nacional Agraria La Molina, Lima, Perú
3
Corresponding author. E-mail: takayuki.ohgue@gmail.com

Abstract

Insect induced galls are not known from bryophytes. Here we report the first occurrence of such galls from thalli of a neo-
tropical liverwort, Monoclea gottschei subsp. elongata (Marchantiophyta: Monocleaceae) from Peru. This is also the first
report of animal-induced galls formed in modern thalloid liverworts. The gall-inducer is a species of the family Agromyzidae
(Diptera). The galls are swellings, but are otherwise indistinguishable from intact thalli as their surface is neither ornamented
nor sclerotized. The histology of the galls, however, suggested that abnormal cell growth and some differentiation occurred
in the parenchymatous cells of the thalli during gall formation.

Key words: bryophyte feeder, Diptera, histology, Monoclea, plant gall

Introduction

Plant galls are primarily induced in vascular plants by various animals, such as nematodes, mites, insects, as well as
fungi and bacteria (Mani 1964), exhibiting great morphological diversity. The gall-inducing insects represent much
of the diversity of plant-feeding insects, and often induce complex gall architecture (Mani 1964; Redfern 2011). They
are generally host-plant specific insects (Shorthouse et al. 2005), and their intimate interactions with plants have likely
accelerated the adaptive radiation of gallers (Price 2005).
Bryophyte galls are extremely rare (Mani 1964). The organisms known to induce galls in bryophytes include
cyanobacteria (Mani 1964), fungi (Martínez-Abaigar et al. 2005; Nour-El-Deen 2011) or nematodes (Dixon 1905;
Glime 2013), with nematodes accounting for most bryophyte galls (Gerson 1982). Among bryophytes, nematode galls
occur mostly on mosses (Glime 2013) and some leafy liverworts (Akiyama 2010; Asthana & Srivastava 1993; Kitagawa
1974; Marchal 1906), and thus so far, are not known from thalloid liverworts or hornworts, although minutes galls
that might have been induced by mites occurred on a thalloid liverwort from the Middle Devonian, Metzgeriothallus
sharona (VanAller Hernick et al. 2008; Labandeira et al. 2014).
Although bryophytes are seldom used as food (Gerson 1969, 1982), they are susceptible to herbivorous insects
with a variety of feeding modes, including external foliage feeding (Smith et al. 2002), leaf-mining (Imada & Kato
2016) and piercing-and-sucking (Min & Longton 1993). However, galling insects are yet to be found on bryophytes.
Here we report the first observation of the insect-induced galls on a bryophyte.

Materials and methods

Liverworts with insect-induced galls were collected at an elevation of approximately 500 m in a tropical mountain forest
in Tarapoto, San Martin, Peru between November 27–29, 2013, and on October 21 and 22, 2014 and on November
21 and 22, 2015. At the study site, galls were seen only on the common thalloid liverwort, Monoclea gottschei Lindb.
subsp. elongata Gradst. & Mues (Monocleaceae; Gradstein et al. 1992). We collected a total of nine mature galls,
of which seven contained a living fly larva. Some thalli with galls were kept for rearing the gall-inducing insects,
whereas others were immediately fixed in FAA (formaldehyde, acetic acid and ethyl alcohol), for examining their
morphology.

Accepted by Bernard Goffine: 9 Jul. 2017; published: 30 Jun. 2018