佛冈县不同类型橘园柑橘木虱的种群动态

[目的] 明确佛冈县不同类型橘园柑橘木虱的种群动态,为当地柑橘木虱及柑橘黄龙病的防治工作提供科学依据。[方法] 通过2015-2016年的系统调查,对广东省佛冈县砂糖橘园的柑橘木虱种群消长动态进行研究,对比分析了不同处理措施对柑橘木虱种群数量的影响。[结果] 1-3月柑橘木虱发生危害较轻,随着嫩梢增多,其种群数量开始上升,6-9月为种群发生高峰期,期间出现多个发生高峰,10月之后种群数量逐渐进入消退期,种群数量维持在较低水平;2015、2016年佛冈县柑橘木虱的季节性消长动态基本一致,但种群发生量存在明显差别;3种不同类型橘园内柑橘木虱种群发生数量也存在显著差异,常年失管橘园柑橘木虱种群发生数量最高,常规水肥管理橘园次之,二者均显著高于常规水肥管理及化学防治橘园。[结论] 化学防治可在一定程度上控制柑橘木虱的种群数量,及时清理失管橘园对控制柑橘木虱和柑橘黄龙病传播至关重要。     

Establishment of Asian citrus psyllid (<Emphasis Type="Italic">Diaphorina citri</Emphasis>) primary cultures

The Asian citrus psyllid (AsCP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is a highly competent vector of the phloem-inhabiting bacterium Candidatus Liberibacter asiaticus associated with the citrus disease huanglongbing (HLB). Commonly referred to as citrus greening disease in the USA, HLB causes reduced fruit yields, quality, and ultimately tree death and is considered the most serious citrus disease. HLB has become a major limiting factor to the production of citrus worldwide. Studies of HLB have been impeded by the fact that C. Liberibacter has not yet been cultured on artificial nutrient media. After being acquired by a psyllid, C. Liberibacter asiaticus is reported to replicate within the psyllid and is retained by the psyllid throughout its life span. We therefore hypothesized that C. Liberibacter asiaticus could be cultured in vitro using psyllid cell cultures as the medium and investigated the establishment of a pure culture for AsCP cells. Several commercially available insect cell culture media along with some media we developed were screened for viability to culture cells from AsCP embryos. Cells from psyllid tissues adhered to the plate and migration was observed within 24 h. Cells were maintained at 20°C. We successfully established primary psyllid cell cultures, referred to as DcHH-1, for D. citri Hert-Hunter-1, with a new media, Hert-Hunter-70.     

Isolation and characterization of an Isaria fumosorosea isolate infecting the Asian citrus psyllid in Florida

A fungal pathogen that killed adult Diaphorina citri Kuwayama (Asian citrus psyllid) (Hemiptera: Psyllidae) in Florida citrus groves during the fall of 2005 was identified and characterized. Investigation of this pathogen is important because D. citri vectors citrus greening disease (Huanglongbing), which was reported in Florida in 2005. The morphological and genetic data generated herein support identification of the fungus as Isaria fumosorosea Wize (Ifr) (=Paecilomyces fumosoroseus) (Hypocreales: Cordycipitaceae) from the Asian citrus psyllid (Ifr AsCP). Koch’s postulates were fulfilled after the fungus was isolated in vitro and transmitted to healthy psyllids, which then exhibited a diseased-phenotype similar to that observed in the field. Both in vitro growth characteristics and two Ifr AsCP-specific molecular markers discriminated the psyllid pathogen from another local Ifr isolate, Ifr 97 Apopka. These molecular markers will be useful to track the dynamics of this disease in D. citri populations. The potential for utilizing Ifr to complement existing psyllid pest management strategies is discussed.     

Establishment of <Emphasis Type="Italic">Psyllaephagus parvus</Emphasis> and <Emphasis Type="Italic">P. perplexans</Emphasis> as serendipitous biological control agents of Eucalyptus psyllids in southern California

The free-living lemon gum psyllid, Cryptoneossa triangula Taylor, and the lerp-forming spotted gum psyllid, Eucalyptolyma maideni Froggatt (Hemiptera: Psyllidae) are invasive pests of eucalypts in California. In 2007, Psyllaephagus parvus Riek (Hymenoptera: Encyrtidae) was discovered parasitizing spotted gum psyllids and Psyllaephagus perplexans Cockerell was collected from lemon gum psyllids. While neither parasitoid species was purposely introduced, presence of the parasitoids was significantly associated with reduced intensity and duration of population peaks for both psyllid species. Spring peaks were reduced more than fall peaks. We estimated minimum rates of parasitism from the ratio of mummies to live nymphs. Higher parasitism was recorded in coastal than inland locations during the spring, while parasitism was similar for coastal and inland populations in the fall. Logistic regression models suggest parasitoids were the determining factor of psyllid population densities, although physical parameters, such as irrigation, may affect psyllid or parasitoid populations.     

柑橘木虱两地理种群的内共生菌群落组成及传菌能力

柑橘黄龙病（Huanglongbing, HLB）是经柑橘木虱Diaphorina citri传播的最主要柑橘病害之一, 危害严重时能对柑橘产业造成毁灭性的破坏。为了鉴定福建和海南2个地理种群柑橘木虱的内共生菌群落组成, 本研究对16S rRNA部分保守序列进行PCR扩增, 并利用特异性引物对不同内共生菌进行了感染率检测; 另外, 还通过人工接虫的方法, 探索柑橘木虱成虫在带黄龙病菌蕉柑Citrus reticulata cv. Tankan上的获菌能力, 以及带菌柑橘木虱成虫对黄岩蜜橘C. reticulata cv. Subcompressa的传菌能力。研究发现, 这2个地理种群的柑橘木虱含有相同的内共生菌组成, 包括α-Proteobacteria, Wolbachia spp., γ-Proteobacteria, mycetocyte symbionts, β-Proteobacteria, Oxalobacter和β-Proteobacteria, Herbaspirillum, 而且这2个地理种群柑橘木虱的4种内共生菌的携带率均在95%以上。柑橘木虱成虫在带菌蕉柑上饲菌28 d后, 带菌率可达到82%, 而带菌柑橘木虱成虫在黄岩蜜橘上传菌75 d后, 可导致橘树整体带菌。本研究为柑橘木虱的进一步研究和防虫治病途径提供了一些理论依据。     

Population Ecology of the Riparian Frog Eleutherodactylus cuneatus in Cuba

A population of the poorly known riparian frog Eleutherodactylus cuneatus was studied for 1 yr along a mountain stream in eastern Cuba. We examined population structure, seasonal and daily activity, growth, and habitat use using mark-recapture and call-point counts. Juveniles were observed during all survey periods with a spike in March. Higher numbers of adults were present in May–July, associated with longer day length, warmer temperatures, and the onset of the rainy season. This was coincident with higher calling activity away from the stream, suggesting an increase in both reproductive and nonreproductive activity in the warmer months between May and September. The number of individuals peaked at 2000–2200 h, but high numbers of individuals were visible throughout the night. Lower activity levels were observed throughout the day. Population size estimates were 84–131 adults and 124–304 juveniles, with averages of 110 and 236 individuals, survival rates were high but capture probabilities were low for a 5-d period in March 2004. Growth rate was negatively related to the size of recaptured individuals, although decreases in growth rate were slight. Frogs were found either in the water (49.7%), or in the banks and on the ground adjacent to the stream where most individuals were found on the ground under the cover of rocks, leaf litter, or large palm fronds. These results provide baseline knowledge of E. cuneatus population dynamics and ecology needed for a rapid detection of any decline this population may undergo in the future.     

Effects of climate,natural enemies and biocides on three citrus mites in coastal New South Wales

Infestations of the citrus rust mitePhyllocoptruta oleivora (Ashmead), the brown citrus rust miteTegolophus australis Keifer, and the citrus red mitePanonychus citri (McGregor), did not cause economic damage to orange (Citrus sinensis (L.) Osbeck) in two coastal New South Wales orchards during a three-year study. The seasonal abundance of the mites and their phytoseiid and coccinellid predators was defined using periodic regressions of transformed counts on time. Population peaks coincided with seasonal rises and falls in temperature and evaporation in late-summer/autumn and in spring/early-summer. Population troughs in late-spring/summer coincided with peaks in temperature and evaporation and reproductive dormancy in some of the coccinellids. Population troughs in winter generally coincided with troughs in evaporation and temperature, particularly in July when the average temperature was about 10°C. Partial correlation coefficients were used to determine the relationships between the predators and their prey. These were mostly nonsignificant atP=0.05. Fortnightly and daily fluctuations in weather did not have any obvious effects on numbers of the mites. The effects of fungicides and pesticides applied during the study were not clear.     

Patterns of habitat use by the Asian citrus psyllid,Diaphorina citri,as influenced by abiotic and biotic growing conditions

相似文献   

柑橘全爪螨种群空间格局的地学统计学分析

应用地学统计学方法分析了柑橘园主要害螨柑橘全爪螨Panonychus citri（McGregor）种群的空间格局及其动态。结果表明,柑橘全爪螨种群具有空间相关性,变程介于1．10～21．0m,其半变异函数主要符合高斯模型,表现为聚集分布,其中3月、8月和9月的聚集强度较大;种群空间格局动态显示,4月、10月为该种群的两个发生高峰期,柑橘全爪螨种群数量快速上升扩散。地学统计学方法能够应用于柑橘全爪螨种群的空间格局分析,并有助于对该害螨进行发生预测与控制处理。     

Population Fluctuation of Three Parasitic Nematodes in Florida Citrus

In Florida, Tylenchulus semipenetrans on citrus has two high and two low population levels each year. High levels occur in April-May and November-December, and low levels, in February-March and August-September. Population increases occur about 4-5 weeks after the spring and fall flush of root growth. Populations of Pratylenchus coffeae on citrus varied widely, and were not related to season. Populations of P. brachyurus showed seasonal variation with a high in June-July and a low in March-May. Males of T. semipenetrans and P. coffeae were found throughout the year, whereas males of P. brachyurus were rare and were found only during November and December.     

The influence of the host plant on the population dynamics of Acizzia russellae (Homoptera: Psyllidae)

Abstract. 1. The role of the host plant, Acacia karroo , in the population dynamics of the indigenous non-pest psyllid, Acizzia russellae , was investigated.
2. Population levels of A.russellae in early summer were almost 10 times greater on the regenerative foliage of pruned trees (cut back in spring) than on normal trees. During late summer and winter, populations declined far more slowly on pruned trees, so that very much higher numbers of psyllids were maintained on these trees through to the next spring. This finding, and others, suggest that natural enemies and climate are not major determinants in the population dynamics of this insect under normal conditions in the field.
3. Laboratory measurements of several chemical and physical characteristics of the foliage of pruned and normal trees did not reveal any differences which would account for the observed effects.
4. Measurements of organic nitrogen concentrations in the leaves of normal A. karroo trees in the field showed significant correlations between psyllid numbers and leaf nitrogen, but only during summer in November and January.
5. Psyllid performance in the laboratory (duration of life cycle, egg production, and dry weight of emergent females) was significantly better for psyllids reared on plants containing high amino nitrogen.
6. It is suggested that the availability of quantities of suitably high quality nutrients in the leaves of pruned A. karroo trees explains the "epidemic" population levels achieved by the psyllid on pruned plants. It seems that characteristics of the host plant impose the major limitation on psyllid population growth, which may explain the permanent low endemic population levels of this insect in the field.     

Lethal and sublethal effects of insecticides on the survival and reproduction of Brevipalpus yothersi (Acari: Tenuipalpidae)

The overuse of insecticides to control vector insects such as Diaphorina citri Kuwayama in citrus groves has altered the population dynamics of pest mites. Among phytophagous mites, population outbreaks of citrus leprosis mite, Brevipalpus yothersi Baker, have been increasingly intense and frequent in Brazilian citrus groves. Despite the great importance of the B. yothersi mite for citrus production, the lethal and sublethal effects of insecticides on this mite have not yet been studied. Therefore, in this study, the effects of insecticides commonly used for D. citri control on B. yothersi mortality, reproduction, and instantaneous growth rate were assessed. For this, two experiments were carried out, one under controlled conditions and another in a greenhouse. The insecticides tested were beta-cyfluthrin, bifenthrin, buprofezin, chlorpyrifos, dimethoate, pyriproxyfen, and thiamethoxam at 0 (control), 0.0625, 0.125, 0.25, 0.5, 1, and twofold the recommended insecticide concentration for D. citri control. The pyriproxyfen insecticide provided high mortality of B. yothersi even at low concentrations. Furthermore, this insecticide negatively interfered with the reproduction of this mite. Beta-cyfluthrin, bifenthrin, buprofezin, chlorpyrifos, dimethoate, and thiamethoxam, in the tested concentrations, showed low impact on citrus leprosis mite. Regarding the reproduction of the mite, no significant increase in fecundity was observed on B. yothersi females exposed to insecticide residues, regardless of the concentration tested. Therefore, the application of these insecticides in the management of pest insects is unlikely to promote an increase in the citrus leprosis mite population.

     

Efficacy and uptake of soil-applied imidacloprid in the control of Asian citrus psyllid and a citrus leafminer, two foliar-feeding citrus pests

The systemic neonicotinoid insecticide imidacloprid, Admire Pro, was applied to 3- and 4-yr-old nonbearing 'Rio Red' grapefruit, Citrus x paradisi Macfad., trees in 2006 and 2007, respectively, to determine its effects in the control of two major citrus pests, the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), and a citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae). Young flush shoots were randomly collected weekly for 13 and 11 wk in 2006 and 2007, respectively, to determine the infestation levels and densities of immature stages of both Asian citrus psyllid and P. citrella. Additional flush shoot samples were collected in 2007 and titers of imidacloprid in leaf tissue were determined using an enzyme-linked immunosorbent assay. Soil application of imidacloprid significantly reduced the infestation levels and densities of both pests on flush shoots, starting from the second week post application. The effects of the neonicotinoid insecticide were similar in both years. Analysis of imidacloprid concentration in leaf tissue showed a gradual increase during the first 3 wk, and titers remained well above 200 ppb for 11 wk postapplication. Significant positive correlations were obtained between imidacloprid titers in leaf tissue and the percentage of control levels achieved for both pests. A high level of suppression of both P. citrella and Asian citrus psyllid populations on citrus trees was associated with imidacloprid titer in leaf tissue >200 ppb, which was reached 2 wk after soil treatment. Although soil application of imidacloprid did not provide rapid knockdown of Asian citrus psyllid and P. citrella populations, it resulted in chronic residues in leaf tissue and long-term suppression of both pests.     

Botanicals,selective insecticides,and predators to control Diaphorina citri （Hemiptera： Liviidae） in citrus orchards

The Asian citrus psyllid （ACP） Diaphorina citri Kuwayama vectors pathogens that cause huanglongbing （HLB） or citrus greening devastating and economically im- portant disease present in most citrus growing regions. Young citrus shoots are required for psyllid reproduction and development. During winter citrus trees produce little or no new growth. Overwintering adults reproduce in spring on newly emerging shoots also attractive to other pests and beneficial insects. Botanicals and relatively selective insecti- cides could help to conserve beneficial insects and reduce pest resistance to insecticides. Sprays of Azadirachtin （Neem）, Tropane （Datura）, Spirotetramat, Spinetoram, and broad- spectrum Imidacloprid were evaluated to control ACP in spring and summer on 10-year-old ＂Kinow＂ Citrus reticulata Blanco trees producing new growth. Psyllid populations were high averaging 5-9 nymphs or adults per sample before treatment application. Nymphs or adults were significantly reduced to 0.5-1.5 per sample in all treatments for 3 weeks, aver- age 61%-83% reduction. No significant reduction in ladybeetles Adalia bipunctata, Ane- glei scardoni, Cheilomenes sexmaculata, and Coccinella septempunctata was observed. Syrphids, spiders and green lacewings were reduced in treated trees except with Tropane. Studies are warranted to assess impact of these predators on ACP and interaction with insecticides. Observed reduction in ACP populations may not be enough considering its reproductive potential and role in the spread of HLB. Follow-up sprays may be required to achieve additional suppression using rotations of different insecticides.     

Analysis of temporal fluctuations in numbers of sexually mature Anastrepha ludens females over an extensive citrus area in northeastern Mexico

The Mexican fruit fly, Anastrepha ludens Loew (Diptera: Tephritidae), is one of the most important pests in citrus‐growing areas in Mexico. In this study, we analyzed the temporal fluctuation of sexually mature females of A. ludens populations with respect to the availability of commercial hosts and climatic factors, as well as population data of females over an extensive citrus area in northeastern Mexico. The numbers of mature females were treated as proportions and analyzed with generalized linear mixed models with a binomial error distribution. Results revealed positive effects on proportions of mature females when commercial hosts (Valencia orange and grapefruit) were available at both medium and high levels, whereas negative effects on proportions were observed when commercial hosts were scarcely available. Monthly analyses indicated positive trends on proportion in March, April, October, and November, whereas negative trends were seen in January and June. A low capture of mature females during the late summer and the onset of winter suggests transitional phenological processes across the year. Overall, no relationships were observed between proportions with temperature and the total number of females; however, a positive relationship was observed between proportion and rainfall. These findings provide insight into the reproductive phenology of A. ludens with practical implications for fruit sampling, as well as for the autocidal or chemical control in an areawide integrated pest management (AW‐IPM) approach in citrus‐growing areas of northeastern Mexico.     

Morphology and function of ovipositorial and tarsal sensilla of female Asian citrus psyllid

The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera:Psyllidae), is one of the most important pests of citrus plants worldwide, due to be the dominant vector of the devastating citrus disease Huanglongbing (HLB). Selection of suitable oviposition site is a crucial event of phytophagous insect life. Usually, the chemical and physical characteristics of a host plant were recognized by sensilla on the ovipositor and tarsi of a phytophagous insect after settling on a plant surface. In this study, the morphology, number, and distribution pattern of the ovipositorial and tarsal sensilla of adult female psyllids, were observed by scanning electron microscopy (SEM) techniques. The effect of these sensilla on oviposition was investigated by sensilla deactivation using hydrochloric acid (HCl). The results showed that sensilla trichoid (ST), sensilla chaetica (ChS) and sensilla basiconica (SB) were distributed on ovipositor, while sensilla trichoid (ST) were distributed on the external genitalia. Sensilla chaetica (ChS) and basiconica (SB) were mainly distributed on the end of the ovipositor back plate, and on the base of the sternum. On tarsus, sensilla trichoid (ST), sensilla chaetica (ChS), sensilla triangular (TeS) and sensilla ear ball (SE) were observed. However, whole tarsal segments were covered with Böhm's mane, which was arranged in a circular line. Oviposition assay revealed that a significantly lower number of eggs were laid on the Murraya paniculata seedlings confined by the psyllids with deactivated ovipositorial sensilla followed by protarsal sensilla, mesotarsal sensilla and hindtarsal sensilla. These results suggested that the ovipositorial and tarsal sensilla of citrus psyllid have an important role in the oviposition.     

华南地区柑橘木虱与柑橘粉虱内共生菌检测及其Wolbachia共生菌的系统发育关系分析

【目的】探明不同地理种群的柑橘木虱Diaphorina citri Kuwayama和柑橘粉虱Dialeurodes citri Ashmead体内昆虫内共生菌的种类及其感染率,并以Wolbachia共生菌为代表,对其系统发育关系进行分析,为今后自共生菌角度研发柑橘木虱和柑橘粉虱的新型防控技术奠定基础。【方法】以16S r DNA、23S r DNA以及wsp为目标基因,利用PCR技术检测采自于广州、湛江、南宁、桂林、厦门的柑橘木虱以及采自广州的柑橘粉虱体内共生菌的种类及其感染率;利用多位点序列分型(MLST)技术和MEGA 5.0软件对不同昆虫样本中的Wolbachia进行系统发育关系分析。【结果】本研究采集的柑橘木虱和柑橘粉虱均含有原生共生菌Portiera和次生共生菌Wolbachia、Cardinium、Rickettsia,但该3种次生共生菌在不同木虱与粉虱种群的感染率有所不同;Arsenophonus只在广州和湛江种群的柑橘木虱中检出。基于wsp基因及MLST基因序列的Wolbachia系统发育分析表明,华南地区柑橘木虱和柑橘粉虱体内的Wolbachia均属于Wolbachia的B大组Con亚组。【结论】不同地理种群的柑橘木虱与柑橘粉虱体内感染的共生菌种类及其感染率不同;Wolabchia共生菌与柑橘木虱寄主不存在协同进化关系,在同一采集点存在Wolbachia通过柑橘寄主在柑橘木虱之间、柑橘木虱与柑橘粉虱之间水平传播的可能性。     

Host plant growth characteristics as determinants of abundance and phenology in jumping plant-lice on downy willow

1. Salix lapponum host plants at an upper altitudinal site differed significantly in size, structural density, phenology, growth performance, and spatial isolation from those growing at a lower site. 2. Plant differences were paralleled by significant differences in psyllid population density and phenology parameters, with psyllid population density, percentage of catkins occupied, and phenological development relatively lower or retarded at the upper site. Population densities at the upper site, nevertheless, remained high. 3. Plant measurements were good predictors of insect density, often explaining up to 73% of the variance in abundance among plants at a given site. 4. Sets of four plant characters identified by best subsets regression were better predictors of psyllid density and development than single factors, although differences were often not great and the combinations of characters selected by multiple regression sometimes differed from the best single predictors. 5. Best single predictors of psyllid density on catkins were measurements of plant size, particularly height, length, and basal stem diameter. Shoot density and catkin phenology were occasionally important but plant isolation and prior growth performance were less important. 6. By contrast with density, age structure of the psyllid population was predicted best from plant phenological measurements, notably catkin phenology.     

Population fluctuations and interspecific competition between Tephritid flies attacking fruit crops in the New Valley oases,Egypt

Population fluctuations of the Mediterranean fruit fly Ceratitis capitata (Wiedemann) and the peach fly Bactrocera zonata (Saunders) were monitored with lure trap collections in three provinces in the New Valley oases, Western Desert, Egypt. Results showed marked temporal differences in peak trap catches of the two flies in the selected sites all over the entire studied areas. One annual peak of C. capitata was recorded during both October 2005 and February 2006 and coincided with the ripening period of citrus trees in Kharga oases. However, two annual peaks were recorded during June and September 2005 in Bodkholow province and coincided with the ripening period of apple and mango. On the other hand, two annual peaks of B. zonata were recorded in Kharga oases throughout May and September and coincided with the ripening periods of apricot, mango and guava. One annual peak only was recorded in the round up of September and/or October in both Moot and Bodkholow in Dakhla oases and coincided with the ripening period of mango, guava and citrus. The occurrence of C. capitata was very limited in comparison with B. zonata. Population fluctuations of the two pests in the studied sites were significantly different. The ability of the traps used in capturing both C. capitata and B. zonata indicated that the yellow sticky trap was more effective in capturing C. capitata. However, the Abdel-Kawi trap was significantly efficient at trapping B. zonata. The occurrence of B. zontata in high numbers all over the study period compared to C. capitata is considered as good proof that this invading fly may be considered as a vigorous competitive tephritid fly to the native fly C. capitata.     

Seasonal flight activity by the Asian citrus psyllid in east central Florida

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is an important invasive citrus pest in the USA because it vectors a bacterium responsible for huanglongbing, a devastating disease of citrus. Information was lacking on seasonal aspects of flight activity by D. citri, which could have ramifications on psyllid management as well as our understanding of epidemiology of the disease. Of interest from a pest management standpoint would be whether D. citri regularly disperses to or away from citrus on a predictable schedule. In research presented here, seasonal flight activity by D. citri was investigated using yellow sticky traps deployed in citrus trees and in fallow areas adjacent to citrus. Results indicated that flight activity by both male and female D. citri away from citrus can occur at any time of the year with consistent dispersal activity during the spring. The research further indicated citrus is continually subject to infestation by immigrating adults and that there is no time during the year that a citrus grower could be assured immigration would not occur. Growers should be aware that adult dispersal occurs regularly during spring and they should time management tactics accordingly. Adult flight activity 2 m from a citrus tree was more pronounced at 1 m above ground than at 2 or 3 m high. At distances of 8–60 m from trees, numbers of adults on traps were similar among the three heights. Males and females were similar with respect to seasonal flight activity. Numbers of adults captured on traps distant from citrus were not correlated with wind speed, sunlight, or air temperature, but there was some evidence that relative humidity influenced flight activity. Although the D. citri life cycle is dependent on flush, data from these studies did not confirm that psyllid dispersal from citrus consistently increases as citrus flush abundance decreases.