The effects of simulated and natural rainfall on cochineal insects (Homoptera: Dactylopiidae): colony distribution and survival on cactus cladodes

ABSTRACT. 1. The distribution of Dactylopius opuntiae (Cockerell) colonies on Opuntia ficus-indica (L.) Miller cladodes collected during a prolonged drought, was recorded for the proximal and distal portions of the cladodes, for the exposed and sheltered surfaces, the edges, and in relation to the proximity of the colonies to areoles at the base of the thorns.
2. Most of the colonies were found on the more sheltered parts of the cladodes and a disproportionately large number of the colonies on exposed surfaces had settled below the areoles.
3. Individuals in colonies on the exposed surfaces were all protected by a relatively hard, compacted wax cover and were thus less vulnerable to simulated rainfall than those on sheltered surfaces. Thorns provided some protection from simulated rainfall for individuals in colonies on exposed surfaces, but not for individuals on sheltered surfaces.
4. Natural rainfall greatly reduced the numbers of colonies, but did not significantly change the distribution of the colonies on the cactus cladodes.
5. Rainfall does not explain the observed distribution of D. opuntiae colonies on the cladodes, but does explain the poor performance of cochineal insects as biological control agents of prickly pear cacti in high rainfall areas.     

Wind dispersal and settling of first-instar crawlers of the cochineal insect Dactylopius austrinus (Homoptera: Coccoidea: Dactylopiidae)

Abstract. 1. The efficiency of D.austrinus as a biological control agent depends on successful colonization of the cactus weed Opuntia aurantiaca .
2. Unlike other coccoid insects, the female crawlers (first-instar larvae) of cochineal insects develop long wax fiaments on the dorsal surface of the body that reduce their terminal velocity in air and enhance wind dispersal.
3. Dactylopiid males are dispersed as winged adults and male crawlers of D.austrinus have fewer and shorter filaments than the females and they are blown a shorter distance in a wind tunnel.
4. Vertical and horizontal wind dispersal of D.austrinus from O.aurantiaca in the field is usually very limited, but was greatly improved when crawlers were launched from an elevated 'tower'.
5. Preparatory to dispersal, female crawlers climb to the top of the host plant and 'take-off' from there. This behaviour is most marked in crawlers 2–3 days old at which stage the wax filaments are best developed: the behaviour is never manifest following artificial 'dispersal'.
6. Final settling on cladodes of the host plant is a function of the age of the female crawlers and of the condition of the cladodes.
7. When given a choice, approximately equal numbers of crawlers settled on cladodes that had received high and low fertilizer treatments. More crawlers settled on cladodes that had been kept in the shade than on those kept in the sun, and on basal rather than terminal cladodes.
8. The highest percentage of crawlers settled on cladodes that were 20% dehydrated. Settling success was much lower on more desiccated cladodes.     

胭脂虫寄生对仙人掌生长的影响

从印榕仙人掌(Opuntia ficus-indica Mill)植株高度、新增茎片数量和新增茎片面积3个方面研究不同密度胭脂虫Dactylopius coccus Costa寄生对仙人掌生长量的影响。结果表明:1)胭脂虫寄生对寄主仙人掌有明显的抑制作用,未被寄生的仙人掌株高、茎片数量和茎片面积的增加均明显大于被寄生的仙人掌;2)随着胭脂虫寄生密度的增加,仙人掌植株生长量的增加相应减少,生长高峰期的出现也会相应推迟;3)胭脂虫的寄生密度应控制在1000头/株以下,过大会导致仙人掌的死亡。     

Hiding in plain sight: Cryptic enemies are found on cochineal (Hemiptera: Dactylopiidae), a scale insect of economic and cultural significance

Cochineal is the common name for cactus‐feeding scale insects in the Dactylopiidae. These ruby‐red insects include the domesticated dye insect Dactylopius coccus. Dactylopius coccus and congeners have been introduced around the world, some accidentally, to become pests of prickly pear cactus species (Opuntia), and some intentionally, for dye production or biological control of pest Opuntia. In the northern Sonoran Desert (Tucson, AZ, USA), we studied the enemy complex of D. opuntiae and D. confusus on Opuntia and characterized two cryptic enemies, a coccinellid beetle predator and a parasitoid wasp. (1) Hyperaspis sp. The coccinellid predator Hyperaspis trifurcata shares a niche with a similar, typically all‐black beetle. Morphological data, crossing tests, and phylogenetic results showed the black beetle to be a distinct, undescribed species in the genus Hyperaspis, with a rare spotted phenotype that is similar in appearance to H. trifurcata. Crossing tests among black and spotted forms showed the spotted morph is inherited as a single‐locus dominant allele. (2) Formicencyrtus thoreauini. Rearing of this ant‐like parasitoid wasp (Encyrtidae) in pure culture of D. opuntiae showed it to be a semi‐gregarious primary parasitoid of cochineal. To our knowledge, this is the first confirmed instance of a cochineal parasitoid. Observations of development show early instar larvae keep their posterior end within the egg chorion, attached to an aeroscopic plate with a connection to the cochineal body wall. Late instar larvae are eventually surrounded by a membrane, likely of larval origin. Wasps then pupate in a dry air‐filled chamber within the desiccated scale remains before chewing out as an adult. Both Hyperaspis sp. and F. thoreauini may have restricted distributions. Hyperaspis sp. does not appear to be a member of the cochineal community in Mexico or Texas, and scant records suggest F. thoreauini may also be restricted to the Southwestern USA.     

First study of the biology of Cryptolaemus montrouzieri and its potential to feed on the mealybug Dactylopius opuntiae (Hemiptera: Dactylopiidae) under laboratory conditions in Morocco

Abstract

Dactylopius opuntiae, is known as specific Opuntia cochineal in many countries around the world. This sap-sucking insect was first detected in Morocco in 2014. To address the problem, the feeding potential of different development stages of Cryptolaemus montrouzieri Mulsant, a biological control agent against mealybugs, was investigated on different development stages of D. opuntiae. Fourth instar larvae and adults of C. montrouzieri were the most voracious feeders on different instars of the mealybug. The numbers of mealybug eggs consumed by first, second, third and fourth instar larva and adults of C. montrouzieri were 36.18?±?1.84, 68.08?±?4.17, 280.55?±?5.41, 540.55?±?5.35, 6514.13?±?64.28, respectively. The numbers of mealybug nymphs consumed by the same stages of C. montrouzieri were 35.43?±?1.75, 67.73?±?3.88, 279.85?±?5.58, 539.63?±?5.08 and 6501.7?±?81.94 (first instars) and 34.83?±?1.20, 57.45?±?1.22, 83.80?±?1.92, 213.65?±?3.46 and 6013.23?±?35.46 (second instars), respectively. The corresponding figures for adult female mealybugs were 1.40?±?0.78, 10.65?±?1.83, 18.58?±?1.24, 25.23?±?1.10 and 197.15?±?3.29, respectively. The egg, larval, prepupal, pupal and adult stages occupied 3.36–3.69, 20.21–27.59, 1.31–1.59, 10.62–10.72 and 96.10–102.51?days, respectively when the coccinellid was reared on different stages of D. opuntiae. The results indicate that C. montrouzieri has the potential to be used as a biocontrol agent in Morocco.     

Indirect versus direct effects of grasses on growth of a cactus (Opuntia fragilis): insect herbivory versus competition

Variation in plant performance between microhabitats is usually attributed to direct mechanisms, such as plant physiological tolerances or competitive interactions. However, indirect mechanisms, such as differences in herbivore pressure mediated by microhabitat differences, could create the same pattern of variation. In this study, we investigated the effect of insect herbivore pressure on the growth of the grassland cactus Opuntia fragilis under different regimes of grassland canopy cover. Our purpose was to establish the extent to which canopy cover plays a direct, competitive role versus an indirect, mediatory role in cactus growth. We manipulated aboveground microhabitat, specifically the cover of adjacent grasses. The three treatments were: (1) open canopy, with grass pinned down away from the cactus; (2) shaded canopy, with a partial mesh cage staked over the cactus; and (3) ambient grass canopy. We measured seasonal plant growth and recorded changes in insect herbivore occurrence and damage in relation to cover. Cactus growth, defined as the change in number of live cladodes, was higher in the open than under either treatment where the plant was more shaded (P<0.05). However, allocation to new growth, measured as the proportion of new segments (cladodes) in a patch, did not differ among cover treatments. Thus, the hypothesis that physiological constraints, or competition for light, limited cactus performance in grass is rejected. Instead, we found that both cladode mortality, caused by the larvae of a cactus moth borer (Melitara dentata), and occurrence of the moth were lower in the open microhabitat than in either shaded microhabitat. Thus, higher net growth in the open, unshaded treatment, rather than representing a release from competition for light with grasses, was better explained as an indirect effect of grass cover on the activity and impact of the cactus moth. These results show that indirect effects can lead to a misinterpretation of experimental data on direct effects. These data also contribute to an improved understanding of mixed results in the biological control of weedy cacti. Clearly, future evaluations of the relative importance of physiology, competition, and insect herbivory in plant performance must be environmentally explicit.     

The introduction ofMimorista pulchellalis [Lepidoptera: Pyraustidae] into South Africa for the biological control of jointed cactus,Opuntia aurantiaca 1. Biology and mass-rearing techniques

A laboratory investigation was conducted on a pyraustid moth imported from South America for jointed cactus control. It was found that the moths were crepuscular, with females laying an average of 48±3.5 eggs over a period of 4–8 days. Larvae hatched out at night and usually tunnelled into the terminal ends of cactus cladodes at a site where young cactus growth occurred. The lifecycle was completed inside the cactus, pupation typically occurring in the dry husk of the cladode on which the egg was laid. Mass-rearing of the moth was easy if plants with young cactus growth were used.      

Metabolic profiling of Dactylopius (Hemiptera: Dactylopiidae) species pigments by geographical origin and hosts using multivariate data analysis

The genus Dactylopius includes the group of insects historically used in Mexico as a source of natural red colorant, the cochineal color. Five species of Dactylopius collected in thirteen states of Mexico and two provinces of Argentina were analyzed using high-performance liquid chromatography with a photodiode array detector. This analysis allowed each species to be identified on the basis of differences in their metabolic profiles. Cluster analysis and principal component analysis differentiated the species by localities and host plant. These two multivariate data analysis techniques were complementary and confirmed the grouping of all analyzed Dactylopius samples. For all species, carminic acid, identified by reference to a commercial sample, was the major compound present in significant amounts, making all five species potential sources of colorant. In addition, each species could be differentiated by the presence of other minor compounds.     

Lagged effects of North Atlantic Oscillation on spittlebug Philaenus spumarius (Homoptera) abundance and survival

The North Atlantic Oscillation (NAO) is a large‐scale pattern of climate variability that has been shown to have important ecological effects on a wide spectrum of taxa. Studies on terrestrial invertebrates are, however, lacking. We studied climate‐connected causes of changes in population sizes in island populations of the spittlebug Philaenus spumarius (L.) (Homoptera). Three populations living in meadows on small Baltic Sea islands were investigated during the years 1970–2005 in Tvärminne archipelago, southern Finland. A separate analysis was done on the effects of NAO and local climate variables on spittlebug survival in 1969–1978, for which survival data existed for two islands. We studied survival at two stages of the life cycle: growth rate from females to next year's instars (probably mostly related to overwintering egg survival), and survival from third instar stage to adult. The latter is connected to mortality caused by desiccation of plants and spittle masses. Higher winter NAO values were consistently associated with smaller population sizes on all three islands. Local climate variables entering the most parsimonious autoregressive models of population abundance were April and May mean temperature, May precipitation, an index of May humidity, and mean temperature of the coldest month of the previous winter. High winter NAO values had a clear negative effect on late instar survival in 1969–1978. Even May–June humidity and mean temperature of the coldest month were associated with late instar survival. The climate variables studied (including NAO) had no effect on the growth rate from females to next year's instars. NAO probably affected the populations primarily in late spring. Cold and snowy winters contribute to later snow melt and greater spring humidity in the meadows. We show that winter NAO has a considerable lagged effect on April and May temperature; even this second lagged effect contributes to differences in humidity. The lagged effect of the winter NAO to spring temperatures covers a large area in northern Europe and has been relatively stationary for 100 years at least in the Baltic area.     

An exaggerated trait in insects: The prothoracic skeleton of Stictocephala bisonia (Homoptera: Membracidae)

The prothoracic skeleton of Stictocephala bisonia was investigated in adults and fifth-instar nymphs on a gross morphological (SEM, maceration) and light microscopic level. In both nymphs and adults, the prothoracic skeleton consists of the pronotum, episternum, epimeron, precoxale, sternum, trochantin, and two endoskeletal characters (furcal arms and pleural apophyses). In nymphs, the entire pronotum is a single-layered outgrowth of the integument communicating with the body cavity and filled with hemolymph and fat body cells (“spine”); the dorsal and ventral processes and the suprahumeral bud are extensions of this single-layered integument. In adults, the pronotum is composed of (1) a proximal, single-layered part, and (2) a larger, distal, double-layered part (“posterior reduplication”) with two cuticular layers separated by a thin lumen. The posterior reduplication is elevated above the body and forms hollow (air-filled) extensions (e.g., suprahumeral horns). Its two cuticular layers are connected through cuticular columns that appear on the external surface as pits. The lumen between these layers communicates with the body cavity and contains nerves and tracheae. In the lumen of newly eclosed adults, intercellular space, epidermal cells with long processes, and hemocytes with nonlipid granules are present. In the lumen of sclerotized adult pronota, the intercellular space has disappeared, together with definite cell boundaries. Several structures are associated with the external cuticle: two types of innervated sensilla trichodea that articulate in the center of external pits, sensilla campaniformia, sensilla coeloconica, and cuticular canals with exterior openings. The morphogenetic implications of pronotal construction, various aspects of adult prothoracic anatomy, and the value of glands and sensilla for an adaptive interpretation of the pronotum are discussed. J. Morphol. 238:157–178, 1998. © 1998 Wiley-Liss, Inc.     

角蜡蚧和日本龟蜡蚧蜡泌物的超微结构及化学成分分析

采用扫描电镜和气相色谱/质谱联用技术研究了角蜡Ceroplastes ceriferus (Fabricius) 和日本龟蜡蚧C. japonicus Green蜡泌物的超微结构及化学成分。结果表明,这2种蜡蚧分泌蜡质和形成蜡壳的过程基本相似。在1、2龄期分泌的蜡质为“干蜡”,蜡壳为星芒状,虫体周缘的蜡芒均为2大节,与其2个龄期发育相对应,每一个大节又分为若干小节。同时,虫体背面中央蜡质堆积成帽状,也分为均匀的多层。由此说明泌蜡过程具有节律性。虫体周缘与蜡芒对应的突起区上分布着密集的刻点状腺孔,每一个腺孔分泌1根蜡丝,这在以往玻片标本中是观察不到的。雌性第3龄幼虫和成虫期,虫体分泌“湿蜡”,形成龟背状蜡壳,泌蜡腺孔主要为三格腺和四格腺。在肛突区发现了密集的泌蜡腺孔,排列为纵条纹状。从角蜡蚧蜡泌物甲酯化处理样品中检测到14个组分,从直接测试 (未经甲酯化处理) 样品中检测到14个组分;而从日本龟蜡蚧则分别检测到10个组分和25个组分。它们的主要成分是一系列高级的长链饱和与不饱和的烃、脂肪酸、脂肪醇、酯类、醛类以及杂环、多环或大环状化合物。对它们可能的生物生态学功能进行了讨论。     

The effects of stylopisation on the sexual development of Javesella dubia (Kirschbaum) (Homoptera: Delphacidae)

This is the first record of the entomophagous parasite Elenchus tenuicornis (Kirby) parasitizing Javesella dubia (Kirschbaum) in England. The effects of E. tenuicornis on the development of (a) the primary, secondary and tertiary sexual organs, and (b) the body characters of J. dubia are discussed in detail.     

The effect ofMetarhizium anisopliae (DAT F-001) concentration and exposure time on the survival of the subterranean pasture pest,Adoryphorus couloni (Col.: Scarabaeidae)

The virulence of the DAT F-001 isolate ofMetarhizium anisopliae forAdoryphorus couloni was tested by exposing final instar larvae (L3) to concentrations of 10¹ to 10⁷ spores/g in a sand-peat mix for up to 112 days at 20°±2°C. All concentrations were pathogenic to L3 larvae and survival was dependent on concentration and correlated with exposure time. The time to kill 50% of the treated larvae (LT₅₀) ranged from 18.9 days (10⁷ spores/g) to 82.7 days (10¹ spores/g). The effect of DAT F-001 on feeding by L3 larvae was determined by comparing the production and weight of frass pellets/larva/day of untreated control larvae with larvae rolled in sporulating cultures ofM. anisopliae DAT F-001 and DAT F-054 (low virulence). Exposure to, and infection byM. anisopliae DAT F-001 had minimal impact on larval feeding. L3 larvae continued to feed at the same rate as both untreated and DAT F-054 treated larvae virtually until they died.

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Résumé La virulence deM. anisopliae DAT F-001 pourA. couloni a été analysée en exposant des larves L3 à des concentrations de 10¹ à 10⁷ spores/g dans un mélange de sable et de tourbe pendant un maximum de 112 jours à une température de 20°±2°C. Toutes les concentrations sont pathogènes pour les larves L3; la survie dépendait de la concentration et est en corrélation avec le temps d'exposition. Les LT₅₀ sont compris entre 18,9 jours (10⁷ spores/g) et 82,7 jours (10¹ spores/g). L'effet de DAT F-001 sur l'alimentation des larves L3 a été évalué en comparant la production et le poids des fèces/larve/jour des larves non-traitées avec des larves roulées dans des cultures sporulées deM. anisopliae DAT F-001 et DAT F-054 (faible virulence). L'exposition àM. anisopliae DAT F-001 suivie de l'infection a peu d'effet sur l'alimentation des larves. Les larves L3 continuent à s'alimenter au même rythme que les larves non-traitées de DAT F-054, quasiment jusqu'à leur mort.

     

圆唇散白蚁补充生殖蚁的类型与建群能力

摘要: 【目的】为了探讨圆唇散白蚁Reticulitermes labralis补充生殖蚁对巢群稳定和发展的作用。【方法】对野外巢群进行调查研究, 及对婚飞成虫通过雌雄配对与补充生殖蚁隔离巢群进行人工饲养的对比研究。【结果】在野外巢群只发现1对原始蚁王蚁后, 而补充生殖蚁的数量最多可达到689头/巢。圆唇散白蚁有3种类型的补充生殖蚁, 即由工蚁转化来的无翅型补充生殖蚁、若蚁转化来的翅芽型补充生殖蚁和末龄若蚁羽化来的拟成虫型补充生殖蚁。实验室条件下婚飞配对群体和隔离群体建群1个月后的存活率分别为64%和96%。建巢初期婚飞配对群体的子代数目增长缓慢, 2个月时的群体数量为6.3±1.54, 10个月时的群体数量也仅为8.4±1.47; 而隔离建群补充生殖蚁2个月时的群体数量为52.4±6.44, 10个月时的群体数量为164.3±20.85, 都高于婚飞配对群体。 此外, 野外巢群的补充蚁后跟原始蚁后一样都具有发达的卵巢。【结论】在圆唇散白蚁中补充生殖蚁是白蚁巢群主要的繁殖力量, 也是建立新巢群的重要繁殖品级。     

Isolation and characterization of microsatellites in the columnar cactus: Polaskia chichipe and cross‐species amplification within the Tribe Pachycereeae (Cactaceae)

Microsatellite markers were developed for the columnar cactus Polaskia chichipe from central Mexico. After an enrichment procedure and three screening steps 87% of colonies contained microsatellites. A pair of primers for 10 loci (seven polymorphic) were developed, tested and used to estimate variation in samples of 18–45 individuals from the Tehuacan Valley, Mexico. Alleles per locus ranged from two to eight (mean 5.28; SD 2.5). Range of expected heterozygosity values was 0.188–0.797 (mean 0.502; SD 0.25). These loci are particularly useful for more precise evolutionary studies, such as gene flow and breeding systems, for this cactus species.     

Effects of gall volume on survival and fecundity of gall-making aphidsAdelges japonicus (Homoptera: Adelgidae)

The number of larvae reaching maturity within the gall of Adelges japonicus was positively related to gall volume, and the relationship between the number of mature larvae and gall volume did not change with different densities of colonized larvae. The population changes in the bud galls of A. japonicus were surveyed by collecting the galls, which did not suffer predation or parasitism within the galls, from young artificial plantations of Picea jezoensis over two years. In the year when the density of colonized larvae was high, they suffered a 42% mortality within the galls, whereas mortality was nearly zero in the low density year. The numbers of larvae per gall were positively correlated with gall volume. The regression lines of the number of colonized larvae on gall volume did not differ significantly in the regression coefficients between the two years, whereas the intercept was significantly higher in the year when the density of colonized larvae was higher. However, different within-gall mortality nullified this difference, and the regression lines of the number of mature larvae on gall volume had no significant difference both in the regression coefficients and the intercepts. This suggests that the number of mature larvae per gall was limited by available resources within the gall which were positively related to gall volume. In 25% of the galls in which mature larvae inhabited, the space within the galls were completely filled by the larvae, indicating that space was one of the limiting resources. Gall volume also affected the number of adults that emerged from the gall and the potential number of their progeny.     

Effect of sucrose octanoate on survival of nymphal and adult Diaphorina citri (Homoptera: Psyllidae)

Asian citrus psylla, Diaphorina citri Kuwayama (Homoptera: Psyllidae) was detected for the first time in the United States near Delray Beach, FL, on 2 June 1998 and is continuing to spread and multiply throughout southern Florida. This psyllid is the vector of Liberobacter asiaticum, a phloem-limited bacterium that causes citrus greening disease. This pathogen has not been found in the Western Hemisphere to date. Furthermore, high infestation levels of D. citri can impact citrus plant health, fruit quality, or yield. Replicated laboratory and spray booth bioassays were conducted to determine the insecticidal activity of a synthetic analog of natural sugar esters found in leaf trichomes of wild tobacco, Nicotiatna gossei Domin, to nymphal and adult D. citri. Field trials were initiated in Fort Pierce, FL, in 2000 to determine activity of the sugar ester formulation (sucrose octanoate) on D. citri and other citrus pests, including immature Asian citrus leafminer, Phyllocnistis citrella Stainton and mites. Sucrose octanoate rates tested ranged from 400 to 8000 ppm (0.1-2% formulated product). Our data suggest that both nymphal and adult D. citri as well as the mite complex tested would be equally controlled to levels of >90% at the higher concentrations of sucrose octanoate and that good coverage is key to efficacy.     

Effects of metaldehyde and methiocarb on feeding preferences and survival of a slug predator (Pterostichus melanarius (F.): Carabidae,Pterostichini)

The potential for reducing slug populations in crops through predation by generalist carabid beetles is well documented. However, few studies have considered interactions between biological and chemical control agents of slugs. Laboratory assays supported previous findings that the consumption of metaldehyde by slugs (Deroceras reticulatum) leads to increased duration of feeding bouts by carabid beetles (such as Pterostichini) on sub‐lethally affected individuals. However, a similar effect was not found for Pterostichus melanarius exposed to slugs fed on the other widely applied pelleted molluscicide formulation (methiocarb). Examination of beetle survival after consumption of slugs containing molluscicides demonstrated the strong biocidal properties of methiocarb, whereas metaldehyde consumption (ingested through slug predation) did not differ from control slugs killed by freezing. Beetle avoidance of slugs containing a more toxic molluscicide compound and the interaction between slug mucus production and beetle attack rates are discussed.     

Nurse plants vs. nurse objects: effects of woody plants and rocky cavities on the recruitment of the Pilosocereus leucocephalus columnar cactus

BACKGROUND AND AIMS: Most studies on cactus recruitment have focused on the role of woody plants as seedling facilitators. Although the spatial association of cacti with objects had been described, the mechanisms underlying this association remain unknown. The aims of this study were to identify which mechanisms facilitate the establishment of a columnar cactus under the shade and protection of objects and to compare these mechanisms with those involved in plant-plant facilitation. METHODS: Three split-split-plot field experiments were conducted to compare the effects of two microhabitats (inside rocky cavities and beneath plant canopies) on seed removal, germination, seedling survivorship and dry weight. Flat, open spaces were used as the control. For each microhabitat, the effect of seed or seedling protection and substrate limitation were explored; aboveground microclimate and some soil properties were also characterized. KEY RESULTS: The permanence of superficial seeds was greater inside rocky cavities than beneath woody plant canopies or on flat, open areas. Germination was similar in cavities and beneath plant canopies, but significantly higher than on flat, open areas. Seedling survivorship was greater beneath plant canopies than inside cavities or on flat, open spaces. CONCLUSIONS: The mechanisms of plant facilitation are different from those of object facilitation. There are seed-seedling conflicts involved in the recruitment of P. leucocephalus: nurse plants favour mainly seedling survivorship by providing a suitable microenvironment, while nurse objects mainly favour seed permanence, by protecting them from predators.