A New Problem and Old Questions:
Potato Psyllid DAVID R. HORTON, W. RODNEY COOPER, JOSEPH E. MUNYANEZA, KYLIE D. SWISHER, ERIK R. ECHEGARAY, ALEXZANDRA F. MURPHY, SILVIA I. RONDON, CARRIE H. WOHLEB, TIMOTHY D. WATERS, AND ANDREW S. JENSEN
T
he potato psyllid, Bactericera cockerelli (Šulc) (Hemiptera: Triozidae) is a small phloem-feeding insect that develops almost exclusively on plants within the Solanaceae (Fig. 1A). The psyllid was described in 1909 by Karel Šulc from specimens collected in Boulder, Colorado, and is found in Mexico, Central America, the western U.S., and southern Canada, and as an introduction in New Zealand (Wallis 1955, Teulon et al. 2009, Munyaneza 2012). Outbreaks of potato psyllid in North America occurred at regular intervals in potatoes, tomatoes, and peppers beginning in the late 1800s and extending into the mid-1900s, largely along a corridor on both sides of the Rocky Mountains. The outbreaks failed to extend into the Pacific Northwest. That pattern changed dramatically in 2011, when an outbreak of potato psyllid caused massive economic losses to potato growers in Washington, Oregon, and Idaho. Losses were due to a new tuber disorder (“zebra chip”; Fig. 1 B-C), now known to be associated with a bacterium that is vectored by potato psyllid. The historical absence of psyllid problems in the Pacific Northwest means that our understanding of psyllid biology under Pacific Northwest conditions is woefully lacking. The outbreak in 2011, coupled with our limited understanding of psyllid biology in the Pacific Northwest, has contributed to a resurgence in research on the biology of potato psyllid. This research includes a substantial commitment to understanding the psyllid’s ecology under Pacific Northwest conditions. As this research has progressed, we are finding that several questions that frustrated entomologists in the early and mid-1900s have re-emerged. Here, we provide a historical overview of how
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our understanding of potato psyllid biology has evolved, with emphasis on questions about the pest’s infestation of crops in northern growing regions. We will show that issues raised by entomologists in northern growing regions during the early 1900s have rematerialized due to the 2011 outbreak of potato psyllid. These issues include questions of whether the psyllid overwinters in northern growing regions, and whether psyllid arrival in potato fields of the Pacific Northwest includes primarily locally overwintered insects (Nelson et al. 2014). Our studies have led to the discovery of an apparently new plant-psyllid association, which we suggest has implications in how we interpret psyllid colonization of potato fields in the Pacific Northwest. Specifically, we believe that this new host association acts as a “bridge” between the overwintering period and germination of the potato crop, in that it provides a maintenance and reproductive host for overwintered psyllids preceding emergence of the potato crop. As we show, this very “bridge” question frustrated entomologists of the mid-1900s in their efforts to understand psyllid outbreaks in northern growing regions.
Psyllid Outbreaks and Infestations: A Brief History The earliest suggestions that potato psyllid might become a damaging pest of solanaceous plants were made by Šulc (1909) in his description of the psyllid; by Compere (1915, 1916), who described infestations of an ornamental plant, Jerusalem cherry (Solanum pseudocapsicum L.), in San Francisco and Sacramento; and by Crawford (1914), who mentioned in his monograph on the North American Psyllidae that potato psyllids could be found in American Entomologist • Winter 2015
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in the Pacific Northwest
high numbers on some cultivated crops (see the review of Butler and Trumble 2012). Many early to mid-1900s records of psyllid damage to cultivated crops were actually assigned retrospectively to the psyllid (Pletsch 1947), as the observations of damage either preceded the 1909 description of the psyllid, or they comprised plant symptoms not known at that time to be associated with the psyllid. Most early records (preceding 1930) of psyllid outbreaks in potato crops are by inference, as the records are based upon historical accounts of widespread crop declines and foliar damage (“psyllid yellows”) later discovered to be caused by potato psyllid. The association between the yellows disorder and the psyllid was not known until the late 1920s and early 1930s (Richards 1928, Richards and Blood 1933). List (1939) summarized records of widespread damage to tomato crops in Colorado from experiment station observations made in 1898-1906; based upon descriptions of the damage, List (1939) retrospectively assigned the damage to outbreaks of the psyllid. Severe outbreaks of potato psyllid and
Fig. 2. Shading: outbreak regions during early to mid-1900s. Solid lines: perceived western and eastern geographic limits of potato psyllid in mid-1900s. Modified from Pletsch (1947) and Wallis (1955).
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Fig. 1. (A) Adult potato psyllid. (B, C) Discoloration of infected fresh tubers and of tuber slices after frying.
psyllid-associated damage, largely along a north-south corridor on either side of the Rocky Mountains (Fig. 2; shading), were also reported in 1911-12, 1927-28, 1938-39, and 1949 (Pletsch 1947, Wallis 1955). Again, some of these outbreaks antedate the late 1920s-1930s realization that the “yellows” damage was caused by the feeding activities of the psyllid, and the damage was retrospectively assigned by later authors to outbreaks of potato psyllid (Pletsch 1947). Damaging infestations of potatoes in the early to mid1900s irregularly extended into southern and eastern Idaho (Pletsch 1947), but not west of that region (Fig. 2; solid line). Indeed, the accepted wisdom in the 1900s was that potato psyllid did not occur in Oregon and Washington (Pletsch 1947), and it was not until 2009 that the primary literature corrected this misconception (Munyaneza et al. 2009). The perception that potato psyllid was not an important component of the potato fauna in the Pacific Northwest changed dramatically in 2011, when an outbreak of the psyllid in Washington, Oregon, and Idaho caused substantial losses to potato growers. The damage was not due to psyllid yellows, but was instead a new plant disorder. In the mid-1990s and early 2000s, potato and tomato growers in the southern U.S. and northern Mexico began to experience outbreaks of this damage, initially of unknown cause but eventually found to be associated with potato psyllid and a bacterium (Candidatus Liberibacter solanacearum [=psyllaurous]; Hansen et al. 2008, Liefting et al. 2008) that is vectored by the psyllid (reviewed in Crosslin et al. 2010, Munyaneza 2012). Symptoms in tomatoes include chlorosis, stunting or death of plants, and production of small, poor-quality fruit (Munyaneza 2012). Symptoms in potatoes include chlorosis, production of aerial tubers, vine collapse, and discoloration of tubers (“zebra chip”; Fig. 1B-C). Zebra chip was first observed in northern Mexico in 1994, and steadily expanded its range northwards to reach the major potato-growing regions of Washington, Oregon, and Idaho in 2011 (Fig. 3).
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The “Overwintering Problem” Outbreaks of potato psyllid along the Rocky Mountains in the early to mid-1900s (Fig. 2) led to efforts by entomologists to determine the geographic source of psyllids colonizing potato fields in those regions. Much of the uncertainty in understanding colonization of crops in these regions revolved around the question of whether potato psyllid overwintered in those higher latitude regions. Indeed, Pletsch devoted a significant portion of his 1947 monograph on potato psyllid to what he termed the “Overwintering Problem.” In that discussion, Pletsch provided three possible explanations for the late spring appearance of potato psyllid in northern growing regions: (1) dispersal from southern growing regions; (2) escape Fig. 4. Bottlenecks possibly limiting northern residency of potato psyllid. Yellow shading: potato crop.
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Fig. 3: First appearance of zebra chip disease in potatoes (from multiple literature sources).
from local greenhouses; and (3) local out-of-doors overwintering. While it is possible that greenhouses may be an occasional source of potato psyllids in crops (Strickland 1938), it seems unlikely that colonization of crops over a geographically wide region can be attributed to escape from greenhouses (Pletsch 1947). This leaves the local overwintering and dispersal explanations. Local overwintering? The assumption in the mid1900s was that the northern limits of potato psyllid were governed by the psyllid’s inability to survive freezing temperatures, combined with a shortage of host plants suitable for survival of psyllids in early spring preceding the potato crop (Pletsch 1947, Wallis 1955). Thus, two bottlenecks were assumed to dictate how far north the psyllid could overwinter (Fig. 4). First, overwintering in northern latitudes would require the psyllid to be cold-hardy enough to survive winter temperatures (Fig. 4). Many north-temperate psyllid species overwinter as diapausing adults on “shelter” plants such as conifers (Hodkinson 2009) and then recolonize host species in late winter or early spring following overwintering. Efforts to confirm this overwintering tactic for northern populations of potato psyllid were unsuccessful (Pletsch 1947, Wallis 1955). Potato psyllid has been collected from conifers in April–June at locations in Arizona, California, and Nevada (Crawford 1914, Klyver 1932, Jensen 1954), but whether those psyllids had also wintered on conifers is unknown. Potato psyllid has also been collected in winter from evergreen shrubs in Nevada and Utah (Klyver 1931, Jensen 1951), but whether the insect shows this tactic in more northern latitudes is not known. Wallis (1955) and Pletsch (1947) caged potato psyllid on coniferous species in late October and late November to examine winter survival in Nebraska and Montana, but were unable to find living psyllids the following spring; Wallis noted that all psyllids in his Nebraska trial failed to survive beyond January. Observations by Daniels (1937) that potato psyllid in Nebraska overwintered on red cedar (Juniperus) received consideration (Hartman 1937, List 1939, Wallis 1941, Pletsch 1947), until it was later shown that those wintering observations were actually for a species of
Fig. 5. Possible route of northern dispersal from southern wintering region (oval). Based upon text in Romney (1939) and Wallis (1941, 1955).
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Aphalara mistakenly identified as potato psyllid (Wallis 1955). In sum, difficulties in finding overwintering populations of potato psyllid at northern latitudes led to the conclusion by entomologists of the early to mid-1900s that the psyllid probably could not survive winter temperatures at those latitudes (Strickland 1938; Wallis 1946, 1955). The second bottleneck perceived to limit residency in northern growing regions is the availability of plants on which the psyllid can survive between the end of overwintering and the emergence of potato in spring (Fig. 4). That is, as temperatures warm in late winter, overwintered psyllids presumably require a plant host suitable for feeding and survival, to act as a “bridge” between overwintering and emergence of the potato crop. Adult potato psyllids can survive for several weeks on plant species that fail to support nymphal development, and it has been suggested that these species, if available suitably early in spring, might contribute to psyllid maintenance and survival until crop emergence (Knowlton 1933). Of more interest, however, has been the question of whether there are plant hosts available preceding crop emergence that also support psyllid reproduction and development. Entomologists in outbreak states struggled extensively with this question (Wallis 1946, 1955; Pletsch 1947). Studies in northern growing regions showed that potato psyllid could be collected on potato or tomato crops as early as the first week of June (Richards 1928, 1929 [northern Utah]; Wallis 1946, 1955 [Nebraska, Wyoming]; Pletsch 1947 [Montana]). Search for non-cultivated solanaceous plants in these regions that were available before late May led to the discovery that the psyllid could be found in spring on some perennial Solanaceae [matrimony vine (Lycium); ground cherry (Physalis)]. While Pletsch (1947) suggested that wild Solanaceae were not abundant enough or were not available sufficiently early in Montana to act as bridge hosts, others suggested that these perennial species might indeed be local spring sources of psyllids moving into crops (Richards 1928, 1929; Knowlton 1934; Daniels 1934; Swenk and Tate 1940; Wallis 1946, 1955). Some of these spring records are as seasonally early as the first or second week of May (Richards 1929, Wallis 1955). Both Knowlton (1934) and Richards (1928) suggested that matrimony vine was available early enough in northern Utah to allow the psyllid to complete a generation on this host before emergence of the potato crop. Dispersal from southern wintering regions? Even with the discovery that potato psyllid could be found on non-cultivated Solanaceae preceding emergence of potato and tomato crops, it was unclear whether those
early-season psyllids had actually overwintered in those northern locations or had arrived on those spring hosts from elsewhere (Swenk and Tate 1940; Wallis 1946, 1955). Difficulties in finding winter populations of potato psyllid in northern growing regions, combined with a sense that the psyllid was not sufficiently cold-hardy to overwinter under severe winter conditions, contributed to the idea that summer outbreaks of potato psyllid along the Rocky Mountains during the 1900s were caused primarily by arrival of the psyllid from southern wintering regions rather than as a consequence of local overwintering (Fig. 5). This idea evolved largely from a 1939 publication by Romney, which describes psyllid phenology on species of Lycium during winter and spring in southern Texas and southern Arizona (Fig. 5; blue oval). Romney found that potato psyllid peaked in numbers on Lycium in late April and early May, but then disappeared from that host by midJune as temperatures increased. The psyllid then reappeared on Lycium in October and November, followed by winter and spring reproduction. Romney interpreted the May–June disappearance of potato psyllid from this winter/spring host to be due to northward dispersal by the psyllid into cooler regions. The idea that summer infestation in northern latitudes might be a function of dispersal has received a great deal of discussion both historically and currently (Wallis 1946, 1955; Jensen 1954; Butler and Trumble 2012; Nelson et al. 2014). Experimental evidence in support of this hypothesis, however, is lacking (Nelson et al. 2014). Wallis (1946, 1955) offered several lines of circumstantial evidence in support of a dispersal hypothesis: (a) potato psyllid has been captured high in the atmosphere (Glick 1939); (b) the psyllid could not be found during winter at northern latitudes; (c) cage studies failed to demonstrate winter survival; (d) potato psyllid was regularly captured in traps in northern latitudes simultaneously with insect species known to disperse from southern wintering grounds; and (e) potato psyllid disappeared from its winter/spring Lycium host in southern regions coinciding with noticeable increases in psyllid numbers at higher latitudes. However, until we have direct evidence for northward migration by the psyllid in appreciable numbers, support for the idea that dispersal has been the source of summer outbreaks in northern growing regions remains circumstantial (Nelson et al. 2014).
Pacific Northwest infestation and a new look at the “overwintering problem” The Haplotype Complication The idea that infestations of potato psyllid in northern growing regions might be associated with dispersal is 237
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A fourth haplotype (Southwestern) has since been discovered (Swisher et al. 2014b), collected from New Mexico, Colorado, and Texas.
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often occurs in association with psyllids of the Western haplotype in potato fields of Washington and Oregon (Fig. 7; Swisher et al. 2012, 2013a, 2014a). However, the Northwestern haplotype has never been collected from outside of the Pacific Northwest, suggesting that it overwinters in the Pacific Northwest rather than arriving there as a migrant from southern regions. Seasonal timing of arrival by potato psyllid in potato fields of Washington is similar to that noted during the 1900s in potato or tomato crops of Montana, Wyoming, Nebraska, northern Utah, and Colorado (Richards 1928; Wallis 1946, 1955; Pletsch 1947). Potato psyllid begins to appear on yellow sticky cards placed in potato fields of Washington in late May to early June (Fig. 8). Psyllids are captured in but a small percentage of fields until late June. By the middle of July, psyllids can be captured on sticky cards in a large percentage of potato fields, with that percentage increasing rapidly as the season progresses through August towards harvest (Fig. 8). These seasonal patterns are also similar to phenology of potato psyllid in southern Idaho, where the psyllid begins to colonize fields in early June (Wenninger et al. 2013). In sum, molecular work and monitoring studies prompt three not mutually exclusive hypotheses for the occurrence of potato psyllid in potato crops of the Pacific Northwest (Fig. 9). The hypotheses include the historical suggestion that potato psyllids (Central haplotype) disperse in large numbers northwards along the Rocky Mountains, arriving in northern growing regions in summer (Fig. 9; blue arrow). Second, repeated discovery of Western haplotype psyllids in Washington, Idaho, and Oregon potato fields (Fig. 7) suggests that this haplotype may also disperse northward from southern regions, possibly along a second route of dispersal (Fig. 9; green arrow). Third, psyllids of at least one haplotype (Northwestern) overwinter in the Pacific Northwest (Fig. 9; red oval) and apparently disperse into potato fields from local overwintering sites as the potato crop emerges. The absence of records for the Northwestern haplotype from outside of the Pacific Northwest supports the idea that this haplotype is resident in the Pacific Northwest, as do wintering observations summarized in the next section. Whether the Central and Western haplotypes overwinter in the Pacific Northwest is still uncertain.
Search for a “Bridge” Host in the Pacific Northwest With the realization that at least one haplotype of potato psyllid is resident in the potato-growing regions of the Fig. 7. Haplotypes of potato psyllid collected late season from potato fields in Washington, Oregon, and Idaho (modified from Swisher et al. 2014a). Red: Northwestern haplotype; green: Western haplotype; blue: Central haplotype. 238
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also being newly debated because of recent molecular studies (see Nelson et al. 2014). Liu et al. (2006) showed that psyllids from California and Baja California differed genetically from psyllids of north-central Mexico and the central U.S. (Fig. 6A), leading to their labeling as distinct genetic types, or haplotypes: Western haplotype (green circles) and Central haplotype (blue circles). Molecular analysis in 2011 confirmed that psyllid populations from potato crops in the central U.S. are composed largely of psyllids of the Central haplotype, whereas psyllid populations westward of this region are increasingly of the Western haplotype (Fig. 6B; Swisher et al. 2012). In 2011, a third haplotype (Northwestern) was described by Swisher et al. (2012) from Washington, Oregon, and Idaho (Fig. 6A; red oval). This haplotype diverges noticeably from the Central and Western haplotypes based upon an analysis of DNA sequences (Fig. 6C).1 The Northwestern haplotype
Fig. 6. (A) Discovery of Western (green), Central (blue), and Northwestern (red) haplotypes of potato psyllid (modified from Liu et al. 2006 and Swisher et al. 2012). (B) Haplotype frequencies in samples collected from potatoes in central U.S. and California (modified from Swisher et al. 2012). (C) Phylogenetic analysis of a 446-bp region of the CO1 gene from three Bactericera cockerelli haplotypes (Genbank accession numbers JQ708093-JQ70895) by maximum likelihood (MEGA6); Bactericera maculipennis (Crawford) (Genbank accession number KP223855) is included as outgroup.
Pacific Northwest, we have in a sense returned full circle to the same question raised by entomologists of the previous century (Fig. 4): what “bridge” host supports the psyllid when potato is not available? In 2011, a search was initiated in Washington, Oregon, and Idaho to discover overwintering and early spring hosts of potato psyllid (Jensen et al. 2012). A perennial nightshade, bittersweet nightshade (Solanum dulcamara L.), was found to support autumn, winter, and post-winter populations of potato psyllid in all three states (Jensen et al. 2012, Murphy et al. 2013, Horton et al. 2014b). American Entomologist • Volume 61, Number 4
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Fig. 8. Maps showing results of season-long trapping in central Washington potato fields. Each yellow or blue circle depicts a single field. Blue: no psyllids captured on sticky cards at that location; yellow: at least one psyllid captured on sticky cards at that location. Red oval shows trapping location. Panel at bottom right shows percentage of fields at which sticky cards captured at least one potato psyllid. Figures modified from Wohleb and Waters (2014).
Bittersweet nightshade is an invasive introduction from Europe or Asia with initial records in North America from New England in the early 1800s (Knapp 2013). The species is now common in the northeastern and northwestern United States (Fig. 10). Bittersweet nightshade grows in large stands, often near water and fence lines, and overwinters as a mat of dormant, above-ground stem material (Fig. 10). The species appears to be highly cold-tolerant (Walters et al. 2011). During the winters of 2012–13 and 2013–14, we sampled stands of dormant S. dulcamara at field sites in northern Oregon and central Washington to learn whether psyllids were present, and to determine diapause status of those psyllids. Horton and colleagues have suggested elsewhere that potato psyllid overwinters in a state of temperature-controlled Fig. 9. Three hypothetical routes for infestation of Washington, Idaho, and Oregon potato fields by potato psyllid. 239
Fig. 10. County records for Solanum dulcamara (map) and photographs of S. dulcamara. Lower left: large mat of S. dulcamara along fence line near Boise, Idaho in May; lower right: same location in February. Map created from online county records for S. dulcamara (Early Detection and Distribution Mapping System; http://www.eddmaps.org)
Fig. 11. Number of mature eggs in dissected female psyllids. Psyllids were collected in autumn and winter from natural stands of S. dulcamara in northern Oregon (Hermiston; 2013) and central Washington (Zillah, Sunnyside, Prosser); sample locations shown as red ovals on map. For a given month and location, size of circle is proportional to frequency of females in that egg maturity class. Numbers in parentheses within each panel depict haplotype composition of a subsample of dissected females (NW: Northwestern; W: Western; from data in Swisher et al. 2013b). 240
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quiescence rather than in a true reproductive diapause, possibly as a mixture of ovarian maturities (Horton et al. 2014ab). We were able to collect both female and male psyllids from all sites during the winter months. Dissections showed that overwintering females included specimens containing mature eggs and specimens having immature ovaries (Fig. 11). Size of a bubble in Figure 11 on a given date is proportional to frequency of females in the sample exhibiting that number of mature eggs at dissection. Thus, while most females were found to have immature ovaries, other females contained a large complement of mature eggs and presumably would rapidly become reproductive with warming temperatures. A subsample of the dissected females was examined with PCR to determine haplotype composition of samples. All but two of 338 specimens
were of the Northwestern haplotype (Fig. 11: numbers in parentheses). To obtain a consistently larger sample of wintering psyllids for dissection, we also enclosed stands of S. dulcamara in large (2m x 2m x 2m), organdy-walled cages (Fig. 12), and inoculated the cages with adult potato psyllids. Cages were inoculated in the summers of 2012 and 2013 with several hundred psyllids of the Northwestern haplotype. We then collected psyllids from cages during both winters and dissected females to determine ovarian maturation and to look for presence of spermatophores to determine mating status. Stems of S. dulcamara were collected at intervals and examined for nymphal psyllids, and newly flushed foliage was collected in March to look for egg-laying by overwintered females. Female psyllids were found to overwinter primarily with immature ovaries, but our collections again included females containing small to large numbers of mature eggs (Fig. 13). The majority of females contained spermatophores (Fig. 13; red portion of pie charts), although there were a number of samples in which unmated females were common (Fig. 13; black portion of pie charts). Interestingly, many of these unmated females had a bluish coloration, which we believe is evidence that the specimens had recently molted to the adult stage. Arrows in both panels show dates that these putatively teneral females were collected. Nymphs were collected on dormant stems throughout both winters. Our interpretation of these results is that
summer (Horton unpubl.), and adults of the first spring generation have been collected in May at locations in Washington, Idaho, and Oregon (Jensen et al. 2012, Murphy et al. 2013, Horton unpubl.). In sum, it is apparent that bittersweet nightshade in the Pacific Northwest is a reproductive host for potato psyllid preceding emergence of potatoes in this growing region.
Bittersweet Nightshade and Potato Psyllid in the Pacific Northwest: A New Association?
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The disjointed east-west distribution of bittersweet nightshade in the U.S. (Fig. 10) may indicate that there have been multiple introductions of this invasive plant. Whether these introductions were intentional or accidental is unknown. It has been suggested that the plant was intentionally introduced into North America for its perceived medicinal uses (see discussion in Knapp 2013). The earliest record for S. dulcamara in North America appears to be from the early 1800s in New England (Knapp 2013). The species appears to be of more recent origin in the Pacific Northwest. Herbarium records suggest that S. dulcamara entered the Pacific Northwest possibly in the late 1800s; the oldest herbarium record for the Pacific Northwest appears to be from a collection in 1880 from northwestern Oregon (Fig. 15). The absence of late 1800s or early 1900s herbarium records from the Rocky Mountain corridor (Fig. 15), in contrast to what we see from
Fig. 12. Cages containing infested S. dulcamara; middle panel: summer 2013; bottom panel: late autumn 2013.
wintering nymphs of potato psyllid exhibited bouts of development during intervals of warmer temperatures, which led to production of teneral females during winter months. The winter of 2013–14 was substantially colder than the winter 2012–13 (see gray shading in both panels of Fig. 13), and teneral females were correspondingly difficult to find in 2013–14 (arrows in Fig. 13). Finally, bittersweet nightshade is also an early spring “bridge” host for potato psyllid preceding emergence of the potato crop. In both years of our cage study, eggs were found on newly flushed foliage (Fig. 14) beginning in March (“E” in Fig. 13). In the 2012–13 samples, onset of egg-laying coincided with a burst of egg maturation in dissected females (Fig. 13). We had difficulties finding adult psyllids in February and March of the 2013–14 study, and dissections ended before the onset of egg-laying that year. Nymphs are found on S. dulcamara well into Fig. 13. Number of mature eggs (left axis) in dissected females collected from caged S. dulcamara in 2012–13 and 2013–14. Size of blue circle is proportional to frequency of females in that egg maturity class. Gray shading shows 24-hr upper and lower temperatures (right axis). Pie charts show percentage of dissected females that had been mated (red shading) or that were unmated (black shading). Arrows point to dates putatively teneral females were collected. E: onset of egg-laying on newly flushed foliage. American Entomologist • Volume 61, Number 4
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Fig. 14. Eggs of potato psyllid (arrows) on newly-flushed foliage of S. dulcamara; March 2014.
Conclusions Summer outbreaks of potato psyllid along the Rocky Mountains have confounded entomologists since the early 1900s, due to uncertainties about the geographic source of psyllids colonizing potato and tomato crops in these regions (Pletsch 1947, Wallis 1955, Nelson et al. 2014). The issue is now even more complex than it was last century, given our recent realization that potato psyllid actually comprises a mixture of distinct genetic types (“haplotypes”) that differ in biology and distribution. Entomologists of the mid-1900s realized that an understanding of psyllid outbreaks in northern growing regions required answers to two questions: (1) was the psyllid capable of overwintering in those growing regions?; and (2), if so, what plant species were available to act as a “bridge” for overwintered psyllids preceding emergence of the crop? With the 2011 outbreak of potato psyllid in Fig. 15. Earliest pre-1950 county records for S. dulcamara west of the Plains states (records obtained from multiple on-line herbarium sources). Red font shows 1800s records. 242
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contemporary records (Fig. 10), seems to indicate that S. dulcamara in the western U.S. is expanding southward and eastward from the Pacific Northwest into the psyllid outbreak regions of the 1900s. A 1926 survey in central Utah failed to document presence of S. dulcamara; by 1979, the plant was extremely common in the survey region (Brotherson and Price 1984). It is also suggestive that entomologists of the mid-1900s did not mention S. dulcamara in any of their extensive lists of plants found to host potato psyllid in outbreak locations, even though they were intentionally searching for plant species that might be post-winter bridge hosts (Knowlton and Thomas 1934, Pletsch 1947, Jensen 1954, Wallis 1955). The absence of S. dulcamara from those lists is consistent with the idea that the current distribution of this plant is a function of recent and ongoing geographic spread. If S. dulcamara is indeed a fairly recent introduction
into the western U.S., then the psyllid/host association also should be relatively new. What this might mean as a factor contributing to the evolutionary divergence of the resident Northwestern haplotype from the two non-resident haplotypes (Fig. 6C), or as a factor helping to maintain that evolutionary divergence, is unclear. Laboratory trials have shown that all three haplotypes easily survive and readily oviposit on S. dulcamara (Mustafa et al. 2015). Field observations, in contrast, seem to indicate that S. dulcamara is substantially less acceptable to the Central and Western haplotypes than to the resident Northwestern haplotype. Psyllids collected in 2012 from potato fields in Idaho, Oregon, and Washington were found to comprise a mixture of haplotypes at the end of the growing season (Fig. 7). That mix of haplotypes was not found in collections made from S. dulcamara during the 2012 growing season or during the winter following the 2012 growing season; the S. dulcamara specimens were composed almost entirely of the Northwestern haplotype (Fig. 16). Psyllids collected from uncaged S. dulcamara during the winter of 2013–2014 were also almost exclusively of the Northwestern haplotype (Fig. 11). Whether the absence of the Western and Central haplotypes from winter collections is caused by a lack of autumn movement from harvested potato fields to S. dulcamara, or rather reflects successful colonization of nightshade but a lack of winter survival, is unknown. Laboratory and fieldcage studies have shown that the Central haplotype, at least, survives exposures to very cold temperatures (-10 to -20 °C; Henne et al. 2010, Whipple et al. 2012, Horton et al. 2014b). Results of these cold-tolerance studies may indicate that the absence of Central and Western haplotypes from S. dulcamara in winter is due less to a lack of cold-hardening abilities than to some trait of bittersweet nightshade that limits psyllid arrival and establishment on this plant in a manner not observed for the resident Northwestern haplotype. Additional study will be required to address this idea.
Fig. 16. Haplotypes of potato psyllid collected from S. dulcamara in Washington, Oregon, and Idaho; winter of 2012–13 and growing season (June– Oct) of 2012. Red: Northwestern haplotype; green: Western haplotype. Modified from Swisher et al. (2013b).
Acknowledgments We thank John Capinera and Warrick Nelson for reviewing an earlier draft of this manuscript. Deb Broers and Merilee Bayer assisted with dissections of psyllids collected from nightshade. Partial support for our overwintering studies was provided by the Washington State Potato Commission and by USDA-SCRI (2009-51181-20176).
References Cited Brotherson, J.D., and K.P. Price. 1984. Naturalization and habitat relationships of bitter nightshade (Solanum dulcamara) in Central Utah. Great Basin Naturalist 44: 317-323. Butler, C.D., and J.T. Trumble. 2012. The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae): life history, relationship to plant diseases, and management strategies. Terrestrial Arthropod Reviews 5: 87-111. Compere, H. 1915. Insect notes. The Monthly Bulletin of the California State Commission of Horticulture 4: 574. Compere, H. 1916. Notes on the tomato psylla. The Monthly Bulletin of the California State Commission of Horticulture 5: 189-191. Crawford, D.L. 1914. A monograph of the jumping plantlice or Psyllidae of the New World. Smithsonian Institution, United States National Museum, Bulletin 85. 186 pp. Crosslin, J.M., J.E. Munyaneza, J.K. Brown, and L.W. Liefting. American Entomologist • Volume 61, Number 4
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Idaho, Oregon, and Washington, entomologists find themselves once again having to address these two questions. We have made progress since the 2011 growing season in understanding psyllid biology in the Pacific Northwest, particularly with the realization that an introduced perennial weed, Solanum dulcamara, is an important part of the psyllid’s winter and spring biology. Potato psyllids of the Northwestern haplotype overwinter on this host plant as both nymphs and adults. Overwintering adults included specimens having a complement of fully developed eggs, and other specimens having immature ovaries. Finally, because S. dulcamara becomes available for egg-laying in March, the host plant appears to be a source of a spring generation of psyllids preceding emergence of the potato crop. Additional study to obtain a better understanding of the biology of other haplotypes under Pacific Northwest conditions is needed to further advance our understanding of potato psyllid as a new pest of potatoes in this northern growing region.
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Temporal and spatial analysis of potato psyllid haplotypes in the United States. Environmental Entomology 42: 381-393. Swisher, K.D., V.G. Sengoda, J. Dixon, E. Echegaray, A.F. Murphy, S.I. Rondon, J.E. Munyaneza, and J.M. Crosslin. 2013b. Haplotypes of the potato psyllid, Bactericera cockerelli, on the wild host plant, Solanum dulcamara, in the Pacific Northwestern United States. American Journal of Potato Research 90: 570-577. Swisher, K.D., S.G. Venkatesan, J. Dixon, J.E. Munyaneza, A.F. Murphy, S.I. Rondon, B. Thompson, A.V. Karasev, E.J. Wenninger, N. Olsen, and J.M. Crosslin. 2014a. Assessing potato psyllid haplotypes in potato crops in the Pacific Northwestern United States. American Journal of Potato Research. DOI: 10.1007/s12230-014-9378-8. Swisher, K.D., D.C. Henne, and J.M. Crosslin. 2014b. Identification of a fourth haplotype of the potato psyllid, Bactericera cockerelli, in the United States. Journal of Insect Science 14: DOI:10.1093/jisesa/ieu023. Teulon, D.A.J., P.J. Workman, K.L. Thomas, and M.-C. Nielsen. 2009. Bactericera cockerelli: incursion, dispersal and current distribution on vegetable crops in New Zealand. New Zealand Plant Protection 62: 136-144. Wallis, R.L. 1941. The potato and tomato psyllid. United States Department of Agriculture, Bureau of Entomology and Plant Quarantine, Leaflet E-532. 8 pp. Wallis, R.L. 1946. Seasonal occurrence of the potato psyllid in the North Platte Valley. Journal of Economic Entomology 39: 689-694. Wallis, R.L. 1955. Ecological studies on the potato psyllid as a pest of potatoes. United States Department of Agriculture, Technical Bulletin 1107. 24 pp. Walters, K.R., Jr., A.S. Serianni, Y. Voituron, T. Sformo, B.M. Barnes, and J.G. Duman. 2011. A thermal hysteresis-producing xylomannan glycolipid antifreeze associated with cold tolerance is found in diverse taxa. Journal of Comparative Physiology (B) 181: 631-640. Wenninger, E.J., N. Olsen, M. Thornton, P. Nolte, J. Miller, and A. Karasev. 2013. Monitoring of potato psyllids, Candidatus Liberibacter solanacearum, and zebra chip in Idaho during the 2013 growing season. Proceedings of the 13th Annual SCRI Zebra Chip Reporting Session, San Antonio, TX. (http://zebrachipscri.tamu.edu/files/2014/04/ Proceedings2013.pdf). Whipple, S.D., J.D. Bradshaw, and R.M. Harveson. 2012. Cold tolerance in potato psyllids. Proceedings of the 12th Annual SCRI Zebra Chip Reporting Session, San Antonio, TX. (http://zebrachipscri.tamu.edu/files/2013/04/2012-Proceedings.pdf). Wohleb, C.H., and T.D. Waters. 2014. Potato psyllid and zebra chip update for the Columbia Basin. 2014 WA/OR Potato Conference, Kennewick, WA. David Horton, Rodney Cooper, Joe Munyaneza, and Kylie Swisher are Research Entomologists with USDA-ARS, Wapato, WA. Silvia Rondon is an Extension Entomologist Specialist with Oregon State University, Hermiston, OR. Erik Echegaray and Alexzandra Murphy are Postdoctoral Scholars with Oregon State University, Hermiston, OR. Carrie Wohleb is Regional
Vegetable Crops Specialist, Grant/Adams area, Washington State University, Moses Lake, WA. Tim Waters is Regional Vegetable Specialist, Franklin and Benton Counties, Washington State University, Pasco, WA. Andy Jensen is Research Manager, Northwest Potato Research Consortium, Lakeview, OR. Correspondence should be sent to David Horton at david.
[email protected]. DOI: 10.1093/ae/tmv047 American Entomologist • Winter 2015
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