Entomophthora Planchoniana Research Articles

Factors driving susceptibility and resistance in aphids that share specialist fungal pathogens

Pandora neoaphidis and Entomophthora planchoniana are widespread and important specialist fungal pathogens of aphids in cereals (Sitobion avenae and Rhopalosiphum padi). The two aphid species share these pathogens and we compare factors influencing susceptibility and resistance. Among factors that may influence susceptibility and resistance are aphid behavior, conspecific versus heterospecific host, aphid morph, life cycle, and presence of protective endosymbionts. It seems that the conspecific host is more susceptible (less resistant) than the heterospecific host, and alates are more susceptible than apterae. We conceptualize the findings in a diagram showing possible transmission in field situations and we pinpoint where there are knowledge gaps.

Virulence of Two Entomophthoralean Fungi, Pandora neoaphidis and Entomophthora planchoniana, to Their Conspecific (Sitobion avenae) and Heterospecific (Rhopalosiphum padi) Aphid Hosts.

Pandora neoaphidis and Entomophthora planchoniana (phylum Entomophthoromycota) are important fungal pathogens on cereal aphids, Sitobion avenae and Rhopalosiphum padi. Here, we evaluated and compared for the first time the virulence of these two fungi, both produced in S. avenae cadavers, against the two aphid species subjected to the same exposure. Two laboratory bioassays were carried out using a method imitating entomophthoralean transmission in the field. Healthy colonies of the two aphid species were exposed to the same conidial shower of P. neoaphidis or E. planchoniana, in both cases from a cadaver of S. avenae. The experiments were performed under LD 18:6 h at 21 °C and a successful transmission was monitored for a period of nine days after initial exposure. Susceptibility of both S. avenae and R. padi to fungal infection showed a sigmoid trend. The fitted nonlinear model showed that the conspecific host, S. avenae, was more susceptible to E. planchoniana infection than the heterospecific host R. padi, was. In the case of P. neoaphidis, LT50 for S. avenae was 5.0 days compared to 5.9 days for R. padi. For E. planchoniana, the LT50 for S. avenae was 4.9 days, while the measured infection level in R. padi was always below 50 percent. Our results suggest that transmission from conspecific aphid host to heterospecific aphid host can occur in the field, but with expected highest transmission success to the conspecific host.

Biodiversity of Entomopathogenic Fungi Naturally Infecting Cabbage Aphid, Brevicoryne brassicae. L.

Ten entomopathogenic fungi were recorded naturally associated with cabbage aphid. They were five hyphomycetes and five Zygomycetes (four Entomophthorales & one Mucorales). Six genera showed good epizootic beside their safety to plants. They were: Panadora neoaphidis, Conidiobolus obscurus, Neozygites fresenii, Entomophthora planchoniana, Cladosporium cladosporioides and Verticillium lecanii. Efficiency of these entomopathogenic fungi against Brevicoryne brassicae was evaluated under laboratory conditions. P. neoaphidis was the most efficient with LC50: 2.5417x 102 conidia/ml then, V. lecanii which showed LC50 of 3.052x102 conidia/ml followed by C. obscurus which showed LC50 of 3.161×102 conidia/ml, then, N. fresenii which recorded LC50 of 8.536×102 conidia/ml. Then, C. cladosporioides showed LC50 of 23.271×102 conidia/ml, then at last comes E. planchoniana with LC50 of 70.593×102.

Prevalence of entomophthoralean fungi (Entomophthoromycota) of aphids in relation to developmental stages.

Transmission of fungal pathogens of aphids may be affected by the host developmental stage. Brassica and Lactuca sativa L. crops were sampled in Santa Fe, Argentina, to determine the prevalence of fungal-diseased aphids and investigate the differences between developmental stages of aphids. The fungal pathogens identified were Zoophthora radicans (Bref.) A. Batko, Pandora neoaphidis (Remaud. & Hennebert) Humber and Entomophthora planchoniana Cornu. Their prevalence on each crop was calculated. The numbers of infected aphids were significantly different between the different developmental stages on all crops except B. oleracea var. botrytis L. The entomophthoralean fungi identified are important mortality factors of aphids on horticultural crops in Santa Fe. The numbers of infected nymphs and adults were significantly different, nymphs being the most affected developmental stage. © 2015 Society of Chemical Industry.

First records of aphid-pathogenic Entomophthorales in the sub-Antarctic archipelagos of Crozet and Kerguelen

Since the 20th century, the sub-Antarctic islands have suffered an increasing number of biological invasions. Despite the large number of publications on this topic, there is a lack of knowledge on parasitism rates of invasive species and on the role of parasites and pathogens to regulate their populations. Six aphid species have been introduced in the archipelagos of Crozet (Ile de la Possession, 46° 25’ S–51° 51’ E) and Kerguelen (49° 21’ S–70° 13’ E). Five of these species were found infected by entomopathogenic fungi of the order Entomophthorales. All these fungal species are cosmopolitan. Conidiobolus obscurus and Entomophthora planchoniana were the most frequently observed on Ile de la Possession and in Archipel des Kerguelen, respectively. This is the first report of pathogenic fungi of aphids on the sub-Antarctic islands. We discuss these results in the light of our current knowledge of these insect pathogens. Their introduction by aphids surviving on plants during transportation is the most likely hypothesis to explain their presence on these remote islands. Keywords: Natural enemies; introduced species; biological invasion; colonization; Zygomycetes; parasitism. (Published: 8 July 2016) Citation: Polar Research 2016, 35 , 28765, http://dx.doi.org/10.3402/polar.v35.28765

First survey on ecological host range of aphid pathogenic fungi (Phylum Entomophthoromycota) in Tunisia

Summary. The natural occurrence of fungal pathogens of aphids and their ecological host range was investigated in Tunisia from 2009 to 2012. The survey focused on aphid infesting different crops and weeds and included 10 different aphid species. Samples were collected from eight agricultural crops sites belonging to three different bioclimatic zones. Four pathogens from the phylum Entomophthoromycota were found to occur naturally in Tunisian ecosystems: Pandora neoaphidis (Entomophthorales: Entomophthoraceae), Entomophthora planchoniana (Entomophthorales: Entomophthoraceae), Conidiobolus obscurus (Entomophthorales: Ancylistaceae) and Neozygites fresenii (Neozygitales: Neozygitaceae). The occurrence of entomophthoralean fungi depended on the sampling area, the bioclimatic zone, and aphid species. P. neoaphidis and E. planchoniana were the predominant pathogens infecting a wide range of aphid species whereas C. obscurus and N. fresenii were sporadically present on a limited number of aphid species. This study is the first survey on ecological host range of entomophthoralean fungi in Tunisia, and the first documentation of C. obscurus and N. fresenii to occur in Tunisia and Maghreb Region.

The effect of Cry1AB insecticidal protein on the incidence of entomopathogenic fungi infecting aphids on Bt maize

There are substantial discrepancies in risk assessments of transgenic maize in Europe. The aim of the study was to determine the quantitative changes in the proportion of fungi-infected aphids and possible differences in the species composition of entomopathogenic fungi on conventional and genetically modified maize, expressing Cry1Ab protein from Bacillus thuringiensis (Bt). The experiments were performed in Lower Silesia, Poland, in 2008–2010. Three cultivars were used, i.e. DKC 3421 YG (Bt), isogenic non-Bt DKC 3420, and the conventional ‘Bosman’ as a reference. Aphids infected with fungi were counted in situ on 18 plants per plot every two weeks through each of the growing seasons. Additionally, twice a year dead aphids were also collected (60 aphids per treatment) and used for fungi identification. Cry1Ab insecticidal protein had no effect on the incidence of entomopathogenic fungi infecting aphids on Bt maize. The number of fungi-infected aphids and their time of occurrence were similar on the three compared cultivars. The same three or four species of entomopathogenic fungi-infected aphids were found in each treatment. Predominating in all the treatments were Pandora neoaphidis, Entomophthora planchoniana and Conidiobolus thromboides.

Prevalence of entomophthoralean fungi (Entomophthoromycota) of aphids (Hemiptera: Aphididae) on solanaceous crops in Argentina

Solanum melongena L. and Capsicum annuum L. were sampled in Argentina to determine the prevalence of fungal diseased aphids. The pathogens identified were Pandora neoaphidis (Remaudière & Hennebert) Humber and Zoophthora radicans (Brefeld) Batko (Entomophthorales: Entomophthoraceae) on aphids from eggplants; and P. neoaphidis and Entomophthora planchoniana Cornu (Entomophthorales: Entomophthoraceae) on aphids from peppers. The highest fungal prevalence was 45.5% (n=2296) and 98.1% (n=3212) from aphids on eggplants and peppers, respectively. In both crops, significant differences were found on number of infected aphids among developmental stages. P.neoaphidis and E. planchoniana caused epizootics in M. persicae.

Natural occurrence of entomophthoroid fungi of aphid pests on Medicago sativa L. in Argentina

Four species of entomophthoroid fungi, Pandora neoaphidis (Entomophthorales: Entomophthoraceae), Zoophthora radicans (Entomophthorales: Entomophthoraceae), Entomophthora planchoniana (Entomophthorales: Entomophthoraceae) and Neozygites fresenii (Neozygitales: Neozygitaceae) were found to infect Aphis craccivora, Therioaphis trifolii, and Acyrthosiphon pisum and unidentified species of Acyrthosiphon on lucerne in Argentina. Samples were collected from five sites (Ceres, Rafaela, Sarmiento, Monte Vera and Bernardo de Irigoyen) in the province of Santa Fe. In this study, Zoophthora radicans was the most important pathogen and was recorded mainly on Acyrthosiphon sp. Zoophthora radicans was successfully isolated and maintained in pure cultures. This study is the first report of entomophthoroid fungi infecting lucerne (Medicago sativa L.) aphids in Argentina.

Potential plant–aphid–fungal associations aiding conservation biological control of cereal aphids in Argentina

The overall aim of this study was to identify potential associations between aphids and plants as reservoirs of entomophthoralean fungi. A survey of weeds associated with wheat field borders in two different localities was performed over two years, from April 2010 to April 2012 in the Pampeana central region, Argentina. On each sampling date, five individuals of each plant species were randomly selected, and healthy and infected aphids were collected and quantified once a month. The taxonomic identities of both aphid hosts and entomophthoralean fungi were established. Aphid–fungus associations identified as favorable for inclusion in conservation biological control strategies in borders of wheat crops are the following: Sonchus oleraceus (L.)/Hyperomyzus carduellinus (Theobald), Uroleucon sonchi (L.)/Pandora neoaphidis (Remaudière & Hennebert) Humber; S. oleraceus (L.)/H. carduellinus (Theobald)/Zoophthora radicans (Brefeld) Batko; Lamium amplexicaule (L.)/Cryptomyzus korschelti Bôrner/P. neoaphidis, Z. radicans, Entomophthora planchoniana Cornu; Foeniculum vulgare (Miller)/Dysaphis apiifolia (Theobald)/Z. radicans; Morrenia brachystephana Griseb/Aphis nerii Boyer de Fonscolombe/P. neoaphidis and Brassica rapa L./Brevicoryne brassicae (L.)/P. neoaphidis.

Presence of the Aphid,Chaetosiphon fragaefolii, on Strawberry in Argentina

Seasonal abundance of the strawberry aphid complex under different agronomic practices in the outskirts of La Plata, Argentina was studied on strawberry, Fragaria x ananassa Duchesne (Rosales: Rosaceae). Aphid densities were low in strawberry fields in which insecticides and fungicides were used. In addition to Aphis gossypii, Aphis fabae, Mysus persicae and Macrosiphum euphorbiae, the aphid, Chaetosiphon fragaefolii (Cockerell) (Homoptera: Aphididae), was recorded for the first time in this horticultural area. Life history and some demographic parameters were calculated for C. fragaefolii. The mean duration of nymphal stages was 10.44 days, the oviposition period was 11.8 days, and the mean number of nymph/female/day was 2.4 ± 0.3. Demographic parameters analyzed included the net reproductive rate Ro = 14.55 ± 0.096 nymph/female, generation time T=16.91 ± 0.035 days, and the intrinsic rate of increase rm = 0.158 ± (0.004). No parasites were found associated with C. fragaefolli. The pathogenic fungus, Entomophthora planchoniana Cornu (Zygomycetes: Entomophthorales) was the main mortality factor. Although aphids are not the main pests in strawberry fields, C. fragaefolii can be a serious problem because it can transmit several virus diseases of strawberry. Greater knowledge of life history traits and mortality factors of this species is needed in order to design appropriate control strategies.

Pathogenic Fungi and Parasitoids of Aphids Present in Air Captures of Migratory Alates in the Low-latitude Plateau of Yunnan, China

To survey fungal pathogens and parasitoids of aphids in the low-latitude plateau of Yunnan, southwest China, 3,553 migratory alates of Brevicoryne brassicae, Lipaphis erysimi, and Myzus persicae were attracted to a yellow-plus-plant trap from air during a full-year period and individually reared on cabbage leaves for 7-14 d at 18-22 degrees C and L:D 12:12. Among the trapped alates, 19.2% were killed by 10 species of aphid-pathogenic fungi after survival of 2.3 d (range, 1-7 d). Another 2.8% were mummified by the wasps Aphidius gifuensis, Diaeretella rapae, Ephedrus plagiator, and Aphelinus mali after survival of 4.9 d (range, 1-11 d). Most of the mycosed alates (77.8%) died from Entomophthorales predominated by Pandora neoaphidis (42.7%) and Zoophthora radicans (14.5%), followed by P. nouryi, Neozygites fresenii, Conidiobiolus spp., Entomophthora planchoniana, and Z. aphidis in decreasing frequencies. A mitosporic fungus, Lecanicillium lecanii, was found frequently in L. erysimi alates trapped in rainy season. However, B. brassicae alates captured in dry season were infected or parasitized very occasionally. The predeath fecundity of the infected or parasitized alates warranted successful colonization on plants, although greatly reduced, and was well shown by the fitted probability for a given fecundity per capita and the increasing mean size of their progeny colonies. Contagious transmission of the alate-borne mycosis in most of the colonies caused high progeny mortalities within 14 d. The results highlight for the first time the diversity of aphid pathogens and the spread of both pathogens and parasitoids with host dispersal flight in the low-latitude plateau.

Natural control ofDiuraphis noxiaandRhopalosiphum maidis(Aphidoidea) by parasitic entomophthorales (Zygomycota) in Slovakia

Seasonal development of entomophthoralean infection in colonies of Diuraphis noxia and Rhopalosiphum maidis was evaluated on summer barley under conditions of south-western Slovakia in 2001 and 2002. D. noxia was infesting summer barley during both years, while R. maidis was only recorded in 2002. Further three cereal aphids, Rhopalosiphum padi, Metopolophium dirhodum and Sitobion avenae, were also observed on summer barley. Complex of entomophthoralean fungi identified in cereal aphid colonies included four species, Pandora neoaphidis, Entomophthora planchoniana, Conidiobolus obscurus and Neozygites fresenii, with P. neoaphidis as the most prevalent fungus during both years. Two parasitic fungi, P. neoaphidis and E. planchoniana, were identified from D. noxia, but P. neoaphidis was predominant. Infection rate in D. noxia colonies was low, not exceeding 15% and 10% in 2001 and 2002, respectively. Only nine R. maidis individuals were killed with entomophthoralean fungi. The fungi were identified as P. neoaphidis and C. obscurus. No epizootics were observed in the aphid colonies. The fungi could not control development of the aphid populations since they did not appear until high host densities had been established in the crops.

Occurrence of entomopathogenic fungi in migratory alate aphids in Yunnan Province of China

Occurrence of entomopathogenic fungi in migratory alate aphids was investigated by trapping air-borne aphids on cabbage and wheat plants and observing the insects for fungal infection. Potted cabbage and wheat plants put 30 m apart on yellow cloth, were placed on the top of a tall building (six-story building) in Yunnan Province, China away from cultivated fields or other vegetation. Seven species of aphids trapped on the plants collected and monitored for fungal infection in the laboratory at a daily basis from 19 February to 31 December, 2003. Aphids were trapped every day during the experimental period. A total of 3,681 aphids were trapped on cabbage and 3,028 on wheat. Myzus persicae (Sulzer), Brevicoryne brassicae (L.), and Sitobion avenae (F.) were the major aphid species accounting for 94.7 and 93.1% of the insect specimens landing on cabbage and wheat, respectively. Other aphis species encountered included, Acyrthosiphon pisum (Harris), Lipaphis erysimi (Kaltenbach), Pemphigus sinobursaris Zhang, and Rhopalosiphum padi (L.). Preference for host plant played significant role in attraction of aphids, especially of the three major species. Accumulated over the whole experimental period nearly 33% of the aphids landing on cabbage and 37% landing on wheat were infected with fungi. Erynia neoaphidis Remaudiere and Hennebert, Entomophthora planchoniana Cornu, and Beauveria bassiana (Balsamo) Vuilemin were the major fungal pathogens encountered and accounted for nearly 95% of the infested aphids on cabbage and 97% on wheat. Other entomopathogenic fungi encountered included Zoophthora radicans (Brefeld) Batko, Conidiobolus obscurus (Hall and Dunn) Remaudiere, and Neozygites fresenii (Nowakowski), Paecilomyces fumosoroseus (Wize) Brown and Smith, and Aspergillus flavus Link. Although the number of aphids trapped throughout the experimental period did not vary consistently with temperature or humidity, the fungal was directly related to relative humidity. Higher insect mortality, especially due to Entomophthorales, positively related relative humidity.

Natural occurrence of entomopathogenic fungi (Zygomycetes: Entomophthorales) of aphid (Hemiptera: Aphididae) pests of horticultural crops in Argentina

A three-year survey of entomophthoralean pathogenic fungi of aphids from horticultural crops in La Plata, Argentina, was conducted. Nine species of aphids, including Aphis fabae Scopoli, Aphis gossypii Glover, Brevicoryne brassicae (L.), Lipaphis erysimi (Kaltenbach), Macrosiphum euphorbiae (Thomas), Myzus sp., Myzus persicae (Sulzer), Nasonovia ribisnigri (Mosley) and Capitophorus elaeagni (del Guercio) were recorded as hosts of entomopathogenic fungi. Six species of Entomophthorales that infected and killed aphids were found in vegetable crops. The fungal species identified were Conidiobolus obscurus (Hall & Dunn) Remaudiere & Keller, Entomophthora planchoniana Cornu, Neozygites fresenii (Nowakowski) Remaudiere & Keller, Pandora neoaphidis (Remaudiere & Hennebert) Humber, Zoophthoraradicans (Brefeld) Batko and Zoophthora sp. Pandora neoaphidis was the most predominant pathogen of aphids and was found throughout the summer (December–March) 2004. The recovery of C. obscurus, N. fresenii and P. neoaphidis represent first records of these fungi for South America.

Observations on the Occurrence of Entomophthorales Infecting Aphids (Aphidoidea) in Slovakia

The species spectrum of entomophthoralean fungi parasiting aphids was investigated in Slovakia. The surveys focused on aphid fauna occupying both agricultural crops and vegetation at non-crop sites. During the surveys, 15 different entomophthoralean species were identified from 66 aphid species. Of these 15 fungal species, eight had not previously been recorded in Slovakia and one species, Erynia erinacea (Ben-Ze’ev et Kenneth) Remaudiere et Hennebert, had not been recorded previously in Central Europe. New hosts for some parasitic fungi were also recorded. The occurrence of fungal infection and the fungal species spectrum varied with sampling period and sampling area. In general, the fungi were observed parasiting aphid populations from April until November. Pandora neoaphidis (Remaudiere et Hennebert) Humber was the predominant fungal pathogen and could effectively reduce aphid populations. Entomophthora planchoniana Cornu and Conidiobolus obscurus (Hall et Dunn) Remaudiere et Keller were also common pathogens of aphids, but without an epizootic potential. On the other hand, Neozygites fresenii (Nowakowski) Remaudiere et Keller had a strong tendency to establish epizootics in dense aphid colonies, especially in those of the black bean aphid. Other entomophthoralean species observed in the country were considered to be minor aphid pathogens on account of their low occurrence, lower specificity to aphids, or high specificity to a single aphid species. This is the first detailed report to date on the occurrence of Entomophthorales in Slovakia.

Observation on the initial inoculum source and dissemination of Entomophthorales-caused epizootics in populations of cereal aphids.

A total number of 1092 migratory alates were trapped from air in wheat grown area of Yuanyang County, Henan Province from early April through May 2002 in order to confirm the source and dissemination of entomophthoralean inocula to cause epizootics of cereal aphids. Those included 415 Sitobion avenae, 642 Rhopalosiphum padi, 22 Metopolophium dirhodum, and 13 Schizaphis graminum. The trapped alates were daily collected and individually reared for 7 days on wheat plants in laboratory. Of those 341 alates died of fungal infection, taking 31.2% in the trapped alates. These included 224 S. avenae, 106 R. padi, 8 M. dirhodum, and 3 S. graminum. Deaths of all infected alates occurred during the first 5 days and 78.9% of the deaths occurred within the first 3 days. Individual examination under microscope proved that all deaths were attributed to entomophthoralean fungi. Of those Pandora neoaphidis accounted for 84.6%, Conidiobolus obscurus for 9.9%, and Entomophthora planchoniana for 5.5%. Four alate deaths died of cross infection of P. neoaphidis and C. conidiobolus. Based on the high infection rate of the migratory alates trapped from air and the field occurrence of epizootics in populations of cereal aphids during the trapping period, Entomophthorales-caused epizootics were likely disseminated by infected alates through their flight and colonization. This makes it reasonable to interpret worldwide distribution of aphid epizootics, particularly caused by P. neoaphidis that has no resting spores discovered.

Entomophthoralean fungi associated with the common nettle aphid (Microlophium carnosum Buckton) and the potential role of nettle patches as reservoirs for the pathogens in landscape

AbstractPopulations of the common nettle aphid, Microlophium carnosum Buckton, inhabiting nettle patches in an agricultural landscape were surveyed for entomophthoralean infection during 1998, 1999 and 2001. Five pathogenic species were identified from the aphid in the course of the survey. Erynia neoaphidis Remaudière & Hennebert, Neozygites fresenii (Nowakowski) Remaudière & Keller, and Neozygites microlophii Keller affected aphid colonies every year. Two minor pathogens, Entomophthora planchoniana Cornu and Conidiobolus obscurus (Hall & Dunn) Remaudière & Keller, were observed only in 2001.An artificial transmission of the three main fungi was carried out to prove horizontal transmission of infection between the common nettle aphid and different aphid species co‐occurring in landscape. N. microlophii, probably monophagous pathogen, did not infect any of the six recipient aphid species in the experiment. Transmissions of E. neoaphidis and N. fresenii conidia were successful with five and four aphid species, respectively. The average mortality of tested aphids after transmission ranged from 0 to 33.33 % for E. neoaphidis and from 0 to 15 % for N. fresenii.The potential of nettle patches as natural reservoirs for pathogens in the agroecosystem is discussed.

Isolation and in vitro cultivation of the aphid pathogenic fungus Entomophthora planchoniana.

Entomophthora planchoniana is an important fungal pathogen of aphids. Although Entomophthora chromaphidis has been considered a synonym for E. planchoniana, the two species are now separated, and E. planchoniana is reported not to grow in vitro. In this paper, we describe for the first time the isolation and cultivation of this species. Entomophthora planchoniana was isolated from a population of Ovatus crataegarius (Homoptera, Aphididae), which was infected by E. planchoniana only. The isolates did not sporulate, but the sequence of the small subunit rDNA and the restriction fragment length polymorphism patterns of the first part of the large subunit rDNA and the ITS II region confirm that the isolates were E. planchoniana. The isolated fungus grew in a medium consisting of Grace's insect cell culture medium supplemented with lactalbumin hydrolysate, yeastolate, and 10% fetal bovine serum or in GLEN medium with 10% fetal bovine serum. Vegetative cells of E. planchoniana were long and club-shaped and did not stain with Calcofluor, thus suggesting that they were protoplasts.

Geographical Distribution and Host Range of Entomophthorales Infecting the Green Spruce Aphid Elatobium abietinum Walker in Iceland

Entomophthora planchoniana and Neozygites fresenii caused infection in populations of the green spruce aphid, Elatobium abietinum, in Iceland. On this aphid species En. planchoniana was exclusively found in the western part of Iceland, while N. fresenii was exclusively found in the eastern part of Iceland. This discrete and nearly nonoverlapping geographical distribution correlates with the distribution of two different populations of El. abietinum found in Iceland. On other aphid species N. fresenii, En. planchoniana, Pandora neoaphidis, and Conidiobolus obscurus were documented throughout the country. Transmission experiments showed that Pa. neoaphidis and En. planchoniana could infect the eastern population of El. abietinum, although they have never been found on this population in nature. This strongly indicates that there is little or no interaction among El. abietinum, other aphids, and their respective entomophthoralean fungi in the field. Furthermore, this study is the first to record epizootics caused by N. fresenii and En. planchoniana in the subpolar region.