An ancient association? Crickets disperse seeds of an early-diverging orchid

A new study pub­lished in Evol­u­tion Let­ters presents evid­ence of the appar­ently unusu­al seed dis­pers­al sys­tem by crick­ets and camel crick­ets in Apostas­ia nip­pon­ica (Aposta­s­ioideae), acknow­ledged as an early-diver­ging lin­eage of Orch­idaceae. Lead author Dr. Kenji Suet­sugu tells us more. 

Seed dis­pers­al is a key evol­u­tion­ary pro­cess and a cent­ral theme in ter­restri­al plant eco­logy. Anim­al-medi­ated seed dis­pers­al, most fre­quently by birds and mam­mals, bene­fits seed plants by ensur­ing effi­cient and dir­ec­tion­al trans­fer of seeds without rely­ing on ran­dom abi­ot­ic factors such as wind and water. Seed dis­pers­al by anim­als is gen­er­ally a coe­volved mutu­al­ist­ic rela­tion­ship in which a plant sur­rounds its seeds with an edible, nutri­tious fruit as a good food for anim­als that con­sume it. Birds and mam­mals are the most import­ant seed dis­pers­ers, but a wide vari­ety of oth­er anim­als, includ­ing turtles and fish, can trans­port viable seeds. How­ever, the import­ance of seed dis­pers­al by inver­teb­rates has received com­par­at­ively little atten­tion. There­fore, dis­cov­er­ies of uncom­mon mech­an­isms of seed dis­pers­al by inver­teb­rates such as wetas, beetles and slugs usu­ally evoke pub­lic curi­os­ity toward animal–plant mutualisms. 

Schem­at­ic dia­gram of intern­al seed dis­pers­al mutu­al­ism: In return for these seed dis­pers­al ser­vices, many plants provide nutri­tion­al rewards to their seed dis­pers­ers in the form of fleshy fruits.

Unlike most plants, all of the >25,000 spe­cies of orch­ids are het­ero­troph­ic in their early life his­tory stages, obtain­ing resources from fungi before the pro­duc­tion of pho­to­syn­thet­ic leaves. Orch­id seeds, there­fore, con­tain min­im­al energy reserves and are numer­ous and dust-like, which max­im­izes the chance of a suc­cess­ful encounter with fungi in the sub­strate. Des­pite con­sid­er­able interest in the ways by which orch­id flowers are pol­lin­ated, little atten­tion has been paid to how their seeds are dis­persed, owing to the dogma that wind dis­pers­al is their pre­dom­in­ant strategy. Orch­id seeds are very small and extremely light, and are pro­duced in large num­bers. These seeds do not pos­sess an endo­sperm but instead usu­ally have large intern­al air spaces that allow them to float in the air column. In addi­tion, orch­id seeds are usu­ally winged or fili­form, evolved to be poten­tially car­ried by air cur­rents. Fur­ther­more, most orch­id seeds have thin papery coats formed by a single lay­er of non-lig­ni­fied dead cells. It has been thought that these fra­gile thin seed coats can­not with­stand the digest­ive flu­ids of anim­als, in con­trast to the thick seed coats in indehis­cent fruits, which are con­sidered an adapt­a­tion for endozoochory.

Dust-like typ­ic­al orch­id (Cre­mas­tra appen­dic­u­lata var. vari­ab­il­is) seeds with thin papery coats and large intern­al air spaces that are eas­ily dis­persed by wind.

How­ever, it is note­worthy that the sub­fam­ily Aposta­s­ioideae com­monly has indehis­cent fruits (which don’t split open when ripe) with hard, crustose black seed coats. Aposta­s­ioids are the earli­est-diver­ging sub­fam­ily of orch­ids and con­sist of only two gen­era (Apostas­ia and Neuwiedia), with only ~20 spe­cies dis­trib­uted in south­east­ern Asia, Japan, and north­ern Aus­tralia. All Apostas­ia and most Neuwiedia spe­cies invest­ig­ated to date are known to pos­sess ber­ries with hard seed coats. Aposta­s­ioids are also well known for sev­er­al unique traits, such as a non-resu­pin­ate flower (i.e. it doesn’t twist when open­ing) with an actin­o­morph­ic peri­anth (radi­ally sym­met­ric­al out­er part of the flower) and pol­len grains that do not form pollin­ia. These have been con­sidered ances­tral char­ac­ter­ist­ics in orch­ids, giv­en that they are sim­il­ar to those found in the mem­bers of Hyp­ox­idaceae (which is closely related to Orch­idaceae) fam­ily. Sim­il­arly, the pres­ence of an indehis­cent fruit with a thick seed coat, found in most Apostas­ia and Neuwiedia spe­cies can be an ances­tral trait in orchids. 

An Apostas­ia nip­pon­ica plant flower­ing in the wild on Yak­ushi­ma Island, Japan. Although most orch­ids have spe­cial­ized labellum, sta­mens and pis­til fused into a gyn­ostemi­um and pol­len rains uni­fied into pollin­ia, Apostas­ia has solan­um-type flower with a rel­at­ively simple gyn­ostemi­um with anthers that con­tain powdery pol­len grains. 

Here I have stud­ied the Apostas­ia nip­pon­ica (Aposta­s­ioideae) seed dis­pers­al sys­tem in the forest under­story of the warm-tem­per­ate forests on Yak­ushi­ma Island, Kagoshi­ma Pre­fec­ture, Japan. Con­sequently, I present the evid­ence for seed dis­pers­al by crick­ets and camel crick­ets in A. nip­pon­ica. Sim­il­ar res­ults were obtained in dif­fer­ent years, indic­at­ing that this inter­ac­tion is likely stable, at least in the invest­ig­ated site. It prob­ably con­sti­tutes a mutu­al­ism, wherein both part­ners bene­fit from the association—orthopteran vis­it­ors obtain nutri­ents from the pulp and A. nip­pon­ica achieves dis­pers­al of seeds from the par­ent plants. The seeds of A. nip­pon­ica are coated with lig­ni­fied tis­sue that likely pro­tects the seeds as they pass through the digest­ive tract of crick­ets and camel crick­ets. Although neither the crick­et nor camel crick­et can fly, they poten­tially trans­port the seeds long dis­tances owing to their remark­able jump­ing abil­it­ies. Des­pite the tra­di­tion­al view that the minute, dust-like, and wind-dis­persed orch­id seeds can travel long dis­tances, both genet­ic and exper­i­ment­al research has indic­ated that orch­ids have lim­ited dis­pers­al abil­ity; orch­id seeds often fall close to the mater­nal plant (with­in a few meters), par­tic­u­larly in under­story spe­cies. Giv­en that A. nip­pon­ica fruits are pro­duced close to the ground in dark under­story envir­on­ments where the wind speed is low, seed dis­pers­al by crick­ets is prob­ably a suc­cess­ful strategy for this orchid. 

Sequen­tial pho­to­graphs of the crick­et Eulandre­vus ivani con­sumingan Apostas­ia nip­pon­ica fruit (indic­ated by arrows). An entire fruit was con­sumed dur­ing a single vis­it by the cricket. 

Orch­id seeds lack a defin­it­ive fossil record due to their extremely minute size. There­fore, the inter­ac­tion described here provides some import­ant clues as to the anim­als that may have par­ti­cip­ated in the seed dis­pers­al of the ancest­ors of orch­ids. Giv­en that the ori­gin of crick­ets and camel crick­ets pre­cedes the evol­u­tion of orch­ids, they are among the can­did­ates for seed dis­pers­ers of the ancest­ors of extant orch­ids. Owing to many ple­siomorph­ic char­ac­ter­ist­ics and the earli­est-diver­ging phylo­gen­et­ic pos­i­tion, mem­bers of Aposta­s­ioideae have been extens­ively stud­ied to under­stand their flor­al struc­ture, tax­onomy, biogeo­graphy, and gen­ome. How­ever, there is still a lack of inform­a­tion regard­ing seed dis­pers­al in the sub­fam­ily. In this paper, I have doc­u­mented the anim­al-medi­ated seed dis­pers­al of Aposta­s­ioideae mem­bers for the first time. Wheth­er seed dis­pers­al by anim­als (and par­tic­u­larly by orthopter­an fruit feed­ers) is com­mon in these orch­ids war­rants fur­ther invest­ig­a­tion. It is pos­sible that this meth­od of dis­pers­al is an ances­tral trait in Aposta­s­ioideae, giv­en that indehis­cent fruits with a hard seed coat are com­mon with­in the clade. Fur­ther research, such as an ances­tral char­ac­ter-state recon­struc­tion ana­lys­is of more data on the seed dis­pers­al sys­tems of oth­er aposta­s­ioids, can provide deep­er insights into the early evol­u­tion of the seed dis­pers­al sys­tem in Orchidaceae.

Dr. Kenji Suet­sugu is Asso­ci­ate Pro­fess­or at Kobe Uni­ver­sity, Japan. The ori­gin­al study is freely avail­able to read and down­load from Evol­u­tion Letters.