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An aggregation pheromone in the intertidal collembolan Anurida maritima
... They have been first evidenced by their effects, e.g. the fact that a place previously conditioned by the presence of one or more individuals becomes attractive to conspecifics (Mertens and Bourgoignie 1977;Verhoef et al. 1977aVerhoef et al. , 1977bMertens et al. 1979;Joosse and Koelman 1979). When extracted from a conditioned substrate with an appropriate solvent, pheromones were able to reproduce the same phenomenon (Manica et al. 2001). However, these experiments did not demonstrate that the molecules were remotely detected. ...
... Their production is negatively abundance-dependent (Verhoef 1984). They are deposited on the substrate (Mertens and Bourgoignie 1977) and some of them are seemingly volatile, being attractive at distance (Verhoef et al. 1977a;Leonard and Bradbury 1984;Krool and Bauer 1987;Manica et al. 2001; Nilsson and Bengtsson 2004b). They are emitted through the intestine, as being found in the faeces (Verhoef 1984), but probably also through the cuticle, as they were detected in extracts from entire uncrushed individuals (Benoit et al. 2009). ...
... Despite their lack of chemical identification, diverse solubility and polarity properties of some collembolan aggregation pheromones have been established as yet. Those produced by Hypogastrura viatica and O. cincta (Mertens et al. 1979) are soluble in water while those emitted by the semi-aquatic Anurida maritima are insoluble in water but soluble in methanol (Manica et al. 2001). Aggregation pheromones extracted from Cryptopygus antarcticus and Friesea grisea were more soluble in methanol than in water and acetone and were insoluble in hexane (Benoit et al. 2009). ...
The present knowledge on chemical communication in springtails (Collembola), one of the two most abundant invertebrate groups living in soil and environments in tight contact with soil (e.g. plant litter, moss), is reviewed here. Chemical communication in an environment where light is absent or dimmed becomes a prominent driver of trophic and non-trophic interactions between soil organisms at a time when better knowledge on the biological determinants of soil communities is required. Like insects and many other arthropods, collembolan individuals of the same population intercommunicate by pheromones, which allow them to signal a risk or to cluster in places favourable for feeding, mating, moulting and ovipositing. Olfaction is also used to select preferred food and mates. Researches so far conducted allowed to discern common trends in the role and chemical composition of odour blends used by Collembola. However, much more needs to be done before reaching straightforward conclusions about chemical communication issues at evolutionary and community levels, making this domain even more rewarding.
... Aggregation behavior has also been illustrated in several Collembola species in laboratory or field investigations (Mertens and Bourgoignie 1977;Verhoef et al. 1977;Joosse and Koelman 1979;Manica et al. 2001;Schulte et al. 2008;Benoit et al. 2009). Feeding behavior can cause aggregation to some extent (Chernova et al. 2007). ...
... Feeding behavior can cause aggregation to some extent (Chernova et al. 2007). But most studies believe there is an aggregation pheromone (Verhoef et al. 1977;Mertens and Bourgoignie 1977;Manica et al. 2001;Benoit et al. 2009), a chemical signal from the cuticle solvent that provokes aggregation behavior in Collembola. However, the exact chemical composition of the pheromones responsible for Collembola aggregation is unknown. ...
Chemical substances excreted from individuals are regarded as chemo-sensory signals that induce aggregation in Collembola. However, chemical or physiological evidence is required to identify the chemical composition of signals responsible for aggregation behavior. Present study applied solvent extraction and gas chromatograph-mass spectrometer-computer technology to separate and identify the chemical compounds in cuticle extracts from the model Collembola species, Folsomia candida. The occurrence of aggregation behavior was confirmed by conspecific attractiveness using a trap bioassay. Eight chemical compounds were obtained from F. candida’s cuticle solvent. The trap assay detected fatty acid combinations from the body extracts of F. candida that induced attractiveness behavior among conspecific individuals and small molecules with higher concentration induced repellent. However, single sensillum recordings of two thin-wall chemical receptors at the second segment of the distal position of the antenna did not receive any positive responses to fatty acids, either single or in combination. The way F. candida used fatty acid combinations as chemical signal for conspecific aggregating was discussed.
... Greenslade, unpublished observations). Aggregations in such places may be facilitated by a pheromone (Manica et al. 2001) under the control of an intrinsic diurnal rhythm. Archisotoma species may even be able to live within a water film; they also have a dense covering of short chaetae. ...
... They aggregate is groups of a few hundred seeking shelter in crevices and under rocks during high tide and disperse for foraging during low tide (Imms, 1906;Joosse, 1966). This aggregation and dispersion behaviour is a result of an endogenous circatidal clock with a period of 12.4 hours, that ensures synchronisation with the change in tide timings (Manica et al, 2001). The aim of this study was to identify suitable genes that exhibit stable expression through the 12.4 hour circatidal rhythm and could be used as reference genes to study the endogenous circatidal clock in Anurida maritima. ...
The identification of reliable reference genes is required in order to accurately assess the levels of gene expression and understand the genes underlying biological rhythms. Anurida maritima is a commonly found cosmopolitan intertidal collembolan which has an endogenous circatidal clock, which is poorly understood. Basic tools to elucidate the clock, especially at the gene expression level, are not available. To fill this gap we identify potential reference genes for qPCR. Reference genes are the genes that show uniform expression under varying experimental or environmental conditions. In this study, we investigate the expression stabilities of six genes, through the 12.4-hour circatidal rhythm, with the help of the widely used RT-qPCR technique. A web-based tool, RefFinder, that integrates the stability rankings of geNorm, Delta-Ct, Normfinder and BestKeeper, was used to analyse and identify the stability of the genes in focus.
... Greenslade, unpublished observations). Aggregations in such places may be facilitated by a pheromone (Manica et al. 2001) under the control of an intrinsic diurnal rhythm. Archisotoma species may even be able to live within a water fi lm; they also have a dense covering of short chaetae. ...
The Collembola fauna of ten cays of the Swain Reefs (Great Barrier Reef) were sampled in July 1982 and 1983. Marine littoral Collembola were found on all but two cays. Terrestrial Collembola were sampled quantitatively in 1983 on three cays of increasing degrees of vegetation cover. On the largest well-vegetated cay, collembolan numbers were at least twenty-fi ve times higher than on the less well-vegetated cays. Xenylla manusiensis, the overwhelmingly dominant Collembolon among the cays, showed a positive association with organic matter in the sample. A species list for all coral and volcanic islands from which Collembola have been collected in the Great Barrier Reef is supplied with notes on ecology and distribution. Some marine littoral species are recorded here for the fi rst time. A family signature shows that Isotomidae are the relatively most species rich group collected and Symphypleonan families and Entomobryidae the least. Adaptations to a marine littoral life of some species are described. Management options to protect the fauna, especially short-range endemics, are suggested.
... Pheromones that lack volatility are perceived when an insect contacts a substrate to which the pheromone adheres. Such contact pheromones occur in collembolans (Manica et aL, 2001), cockroaches (Nishida et aL, 1979;Nojima et aL, 1999), termites (Henderson, 1998), locusts (McCaffery et aL, 1998), and thysanurans (Tremblay & Gries, 2003). Most of these insects inhabit enclosed microhabitats with little air movement, potentially rendering volatile pheromones less effective than contact pheromones. ...
... Less is known about the physiology of F. grisea, but the two species have considerable overlap in habitat, thus it is likely that this species prefers nearly the same conditions as C. antarcticus. The presence of pheromone-induced aggregations in F. grisea and C. antarcticus is consistent with previous reports for several species of Collembola from the temperate zone ( Hopkin 1997; Manica et al. 2001; Wertheim et al. 2005). Overall, cues triggering gregarious behavior are fairly common among insects and related arthropods (Wertheim et al. 2005). ...
Terrestrial arthropods that reside in Antarctica are exposed to considerable periods of environmental stress, thus factors
that promote identification of favorable microhabitats are extremely important. In this study, we report the presence of chemical
cues that induce oviposition and aggregation in two species of Antarctic collembolans, Cryptopygus antarcticus and Friesea grisea. Responses of the Collembola were enhanced by low temperatures but were not altered by humidity. One of the major physiological
benefits derived from an aggregation was a substantial reduction in water loss rates. Although F. grisea and C. antarcticus were commonly found in cross-species aggregations, we found no evidence to suggest cross-species attraction. When individuals
were exposed to areas previously occupied by groups of Collembola, more eggs were laid. Thus, chemicals released by the collembolans
appear to induce both aggregation and oviposition in these Antarctic species.
... Podurid collembola are often gregarious. Therefore, alarm and aggregation pheromones are important for them (Joosse and Koelman, 1979;Purrington et al., 1991;Messer et al., 1999;Manica et al., 2001). ...
Two phenolic acids were identified in the collembolan Ceratophysella denticulata: 3-hydroxy-4,5 dimethoxy benzoic acid and 4-hydroxy-3,5-dimethoxybenzoic acid (syringic acid). These are localized on or in the integument of the springtail, in field-collected animals, in a ratio of 47:100 (v/v). Springtails kept under different temperature regimes showed differences in production and ratio of the benzoic acid derivatives. At 20 degrees C, C. denticulata produced only syringic acid, whereas at 10 degrees C both isomers in a ratio of 100:61 (v/v) were detected. Bioassays with C. denticulata as well as with the specialized collembolan predator Stenus comma (Staphylinidae) were carried out. Staphylinid beetles topically treated with the acids try to clean their mouthparts by rubbing them on the ground significantly more often than do control beetles. Both compounds individually and as a natural mixture have deterrent effects towards the predator S. comma.
... In insects, the different types of cuticular compounds are functionally involved, particularly in sexual communication [13,14] . In Collembola, intraspecific interactions such as reproductive attraction and recognition signalling [15,16], aggregation [17,18,19,20,21] and alarm [22,23,24] rely heavily on olfactory interactions through chemical compounds. As they also play a major role in sexual recognition [25,26] and thus in premating isolation mechanisms [27] , cuticular compounds , as a type of character, deserve a special attention in the study of groups of subspecific entities. ...
In most Arthropod groups, the study of systematics and evolution rely mostly on neutral characters, in this context cuticular compounds, as non-neutral characters, represent an underexplored but potentially informative type of characters at the infraspecific level as they have been routinely proven to be involved in sexual attraction.
The collembolan species complex Deutonura deficiens was chosen as a model in order to test the utility of these characters for delineating four infraspecific entities of this group. Specimens were collected for three subspecies (D. d. deficiens, D. d. meridionalis, D. d. sylvatica) and two morphotypes (D. d. sylvatica morphoype A and B) of the complex; an additional species D. monticola was added. Cuticular compounds were extracted and separated by gas chromatography for each individual. Our results demonstrate that cuticular compounds succeeded in separating the different elements of this complex. Those data allowed also the reconstruction of the phylogenetic relationships among them.
The discriminating power of cuticular compounds is directly related to their involvement in sexual attraction and mate recognition. These findings allowed a discussion on the potential involvement of intrinsic and paleoclimatic factors in the origin and the diversification of this complex in the Pyrenean zone. This character type brings the first advance from pattern to process concerning the origin of this species complex.
... Another possible explanation for the observed behavior is that Collembola use aggregation pheromones. While some species of Collembola have been reported to produce these odors (Verhoef et al. 1977, Christiansen et al. 1992, Manica et al 2001), we believe that our results were achieved irrespective of any pheromone release. First, other researchers (Heupel 2002, Dromph 2003) who studied avoidance behavior in Collembola showed that aggregation pheromones did not play a major role in their studies. ...
Previous observations have indicated homology in the cellular components between Collembolan eyes and the compound eyes of insects. However, behavioral or physiological studies indicating similarities in function are lacking. Collembolan eyes were examined from three species in the Family Isotomidae using scanning electron microscopy. Collembolan eyes are arranged dorsally and laterally on each side of the head in two species, Proisotoma minuta with eight eyes on each side of the head and Folsomia similis with one eye on each side of the head. In both of these species the eyes were located just posterior to the postantennal organ. In Folsomia candida, no external eye structures were detected. These three species were assayed for a series of behavioral preferences using ultraviolet (UV), white light and dark, and temperature conditions. The tests demonstrated that over 76% of all three species, including the eyeless F. Candida, chose white over UV light, over 69% preferred dark over UV, and over 77% favored dark over white light. The results demonstrated that all three species detect both UV and white light and avoid it, preferring cool, dark habitats. From the results of this study, it is hypothesized that F. candida may, in fact, be only "lensless" and may be able to detect light by having internal, non-ocular photoreceptors. Further histological studies are needed to investigate this possibility.
We tested the hypothesis that aggregation behaviour of the
firebrat, Thermobia domestica (Packard) (Thysanura: Lepismatidae), an
inhabitant of enclosed microhabitats, is mediated, at least in part, by
a pheromone. Individual insects were released into the central chamber
of a 3-chambered olfactometer and test stimuli were placed in lateral
chambers. Paper discs previously exposed for 3 days to 10 female, male,
or juvenile T. domestica were all preferred by female, male, or juvenile
T. domestica over unexposed paper discs, indicating the presence of an
aggregation/arrestment pheromone. In additional experiments, frass and
scales from female T. domestica, tested singly and in combination,
proved not to be the source of the pheromone. Physical contact was
required for pheromone recognition, indicating that the pheromone
arrests rather than attracts conspecifics. Arrestment by the
long-tailed silverfish, Ctenolepisma longicaudata Escherich
(Thysanura: Lepismatidae), but not by the common silverfish, Lepisma
saccharina L. (Thysanura: Lepismatidae), to T. domestica exposed
paper discs suggests closer phylogenetic relatedness between C.
longicaudata and T. domestica, than between C.
longicaudata and L. saccharina. Whether C.
longicaudata or L. saccharina produce an aggregation
signal, and whether T. domestica respond to this signal is unknown.
Female, male, and juvenile firebrats, Thermobia domestica (Packard) (Thysanura: Lepismatidae), employ a pheromone that arrests conspecifics on contact. Paper shelters placed in a T. domestica colony accumulate fecal excreta (= frass) and other insect-derived debris. Such shelters elicit arrestment by conspecifics. However, the definitive source of the arrestment pheromone was not known. We tested the hypothesis that one or more debris components from a T. domestica shelter constitute the source of the arrestment pheromone. In dual-choice, still-air olfactometer experiments, scales, exuviae, antennae, caudal filaments, gregarine parasite cysts, and silk (each intact or macerated) retrieved from shelters and separated for experiments, as well as saliva, hemolymph, and fat body extracted from insects all failed to arrest female T. domestica. Similarly, paper that had been fed upon by insects did not elicit an arrestment response, eliminating insect-altered cellulose as the arrestant pheromone. In contrast, insect-exposed glass significantly arrested females. Moreover, females were significantly arrested by (i) loose, insect-derived debris brushed from shelters, (ii) a frass mixture manually separated from loose debris, and (iii) specific amber-type frass manually separated from the frass mixture. These results lead us to conclude that amber-type frass constitutes the source of at least part of the T. domestica arrestment pheromone.
Arthropod microhabitat selection involves a hierarchical assessment of abiotic and biotic factors. In choice experiments, we tested firebrat, Thermobia domestica, microhabitat preferences. Firebrats preferred elevated (35°C) over ambient (20°C) temperature, black over white shelter, and small (1cm) over large (15.5cm) entrance holes. Food availability did not alter shelter selection by firebrats. Medium juveniles, large juveniles and adults, in homo- and heterogeneous populations, preferred high (4.5 and 6.0mm) over low (1.5 and 3.0mm) shelter heights. Small juveniles, however, selected shelters with conspecifics, not by size. Females held at 35°C, but not 20 or 25°C, laid large numbers of eggs. Thus, abiotic characteristics of a shelter, coupled with the presence of conspecifics, affect microhabitat selection by firebrats. These findings may improve entrapment and management systems of firebrats.
Aggregations of the common silverfish, Lepisma saccharina, and giant silverfish, Ctenolepisma longicaudata (both Thysanura: Lepismatidae), are mediated by species-specific pheromones. In dual-choice, still-air olfactometer experiments, filter paper previously exposed to 12 male, female, or juvenile L. saccharina or C. longicaudata arrested conspecifics regardless of developmental stage or sex. Arrestment responses required physical contact with the pheromone. Insect-derived frass, scales, antennae, and setae, as well as salivary gland content, are not the source of the contact pheromone in L. saccharina. Lepisma saccharina did not respond to the pheromone of C. longicaudata, nor to that of another thysanuran, the firebrat Thermobia domestica. However, C. longicaudata responded to pheromones of both L. saccharina and T domestica, whereas T. domestica responded to the C. longicaudata but not L. saccharina pheromone. These results support the hypothesis that a closer phylogenetic relationship exists between C. longicaudata and T domestica than between C. longicaudata and L. saccharina, but a definitive conclusion must await molecular genetic analyses of all three species.
The intertidal insect Anuridamaritima (Apterygota: Collembola) has a circatidal rhythm of locomotory activity on the soil surface which was observed during both the day and the night. The main function of this activity was foraging for food. When a superabundant food supply was provided on the upper shore, this completely repressed the usual migration to the lower shore. There was a clear rhythm in feeding activity which was highest shortly after the sea uncovered the insects' shelters and declined rapidly during the intertidal period. The circatidal rhythm of locomotory activity persisted in the laboratory in constant light for seven days (15 cycles). A free-running rhythm underlying the degree of aggregation was also detected.
We investigated the cues used by the intertidal insect Anurida maritima (Apterygota: Collembola) to orient to the appropriate zone in which to seek shelter during high tide. Our experiments clearly
ruled out any significant role for magnetic, local topographic, slope or celestial cues. Instead, we suggest that the difference
between the appearance of the up-shore and the down-shore horizon is the major cue used by the collembolans. When a mirror
was used to duplicate either of the two horizons, the insects were not able to orient. The insects moved towards an artificially
dark horizon (the reverse of the mirror) placed down-shore, the opposite of their usual direction of movement. The insects
had an endogenous circatidal rhythm of phototactic behaviour: most of the population was always negatively phototactic, but
between 2 and 7 h after low tide, a significant proportion of the population became positively phototactic. This is the first
demonstration of an endogenous tidal rhythm of orientation in an insect.
Egg development takes 9 days at 20oC sexual maturity is reached in 3-4 wk, and 5 ecdyses, and life span amounts to c9 months (30 ecdyses). Contamination with adult specimens caused aggregation; contamination by young springtails until the 4th ecdyses did not. The aggregation pheromones are thus probably sexual pheromones which ensure encounters of mature specimens. -from Authors
The effect on population growth of interspecific interactions was studied among Folsomia candida, Xenylla grisea, Sinella caeca and Pseudosinella violenta. Interaction was mediated by direct interaction, substrate conditioning and airborne allomones. Results of the interaction between any two species usually varied greatly depending on the mechanism involved. Given the nature of Collembola habits and habitats it is likely that one mechanism will dominate under certain circumstances and another under different ones. -from Authors
In Collembola, pheromones appear to be present in the faecal pellets. Pheromone release after cessation of faeces production points to the digestive tract as a possible site of biosynthesis.During the pre-moulting periods Collembola do not react to pheromones, possibly due to their low activity at that time, whereas the production of the pheromones continues.Starvation periods of up to 14 days diminish pheromone release but do not cause complete cessation. Production per animal seems to decrease at increasing densities.The effect of pheromones on the reproductive efficiency of Collembola is discussed in the context of their physiological and behavioural ecology.
The terms "attractant" and "repellent" only have commonly Been employed to describe chemicals in terms of their effect on the behavior of insects. The two terms as defined in their strictest sense do not apply to all possible types of reactions of insects to chemicals. There is a genuine need to clarify the use of terminology in this subject. An analysis of the behavioral effects of chemicals on locomotion, feeding, and oviposition has led to the designation and definition of five terms; namely, arrestant, stimulant (locomotor, feeding, ovipositional),attractant, repellent, deterrent. It is proposed that these five be employed as standard terms within the limits of the definitions given.
O autor estudou os Colembolos do litoral brasileiro. Coletas e experiências no campo livre foram feitas de Junho a Dezembro de 1960.No litoral rochoso duas espécies são comuns: Anurida maritima e Axelsonia tubifera. As duas espécies apresentam o seu máximo de concentração na parte superior da zona intertidal. Foi estudada a distribuição das duas espécies nos diferentes substratos (rocha livre, zona de Chthamalus, Balanus, Ostrea, Mytilus, Bostrychia e Phragmatopoma). Observações sobre a atividade e experiências sobre a nutrição foram feitas em campo livre com Anurida marítima: Esta espécie é ativa durante a maré baixa não só durante o dia como também durante a noite. Diferentes animais litorâneos mortos (poliquetas, cirripedias, isopodas, lamellibranquias, gastropodas) foram devorados.Na região intertidal do mangue Axelsonia tubifera e Pseudanurida sawayana eram frequentes. No litoral arenoso foi encontrado o genero Archisotoma, mas não Anurida marítima, Axelsonia tubifera e Pseudanurida sawayana.Uma nova espécie, Pseudanurida sawayana n. sp., é descrita. A morfologia de Anurida maritima, especialmente a variabilidade do orgão post‐antenal, é discutida.Interessantes resultados zoogeograficos são: 1. Genero Pseudanurida foi pela primera vêz encontrado no Oceano Atlântico e na America do Sul; 2. Foi provada a existência pela primera vêz de Anurida maritima na America do Sul.
On a marine saltmarsh, the intertidal collembolan Anurida maritima (Gurin) has a well-defined tidal rhythm of activity on the mud surface between submerging tides: a large proportion of the individuals emerge from their underground refuges shortly after the retreat of the tide, forage there for a few hours, and retire underground at least 1 h before the return of the tide. This activity rhythm has a period of about 12.4 h and it persists in the field during sequences of non-submerging tides and in the laboratory away from the tides in constant light. In the field the level of activity is greatly reduced during the night. It is suggested that the function of this tidal rhythm is to enable individual Anurida to anticipate the return of the tide both during periods of regular, twice-daily tidal submergence and after a period of days when the habitat has not been covered by the tide.
A study about the function of the "nests" of Anurida maritima (Guér.) in the vertical clay-walls of some creeks has been carried out. In these nests the animals seek refuge from the incoming tide. They clump together in cavities, which are filled with air during high water. At low tide part of the population wanders over the salt marshes in search of food. Among these animals the females prevail. Another part of the population however, remains in the nests, in which they moult. In some of these nests mainly sexually mature animals can be found, which meet there to deposite the eggs. The eggs hibernate. This is considered to be a diapause. They hatch in April. Weather conditions appeared to have a marked effect upon the animals. Three reactions may be distinguished: 1. During sunshine little exchange of animals takes place between nests and marshes. 2. Disappearance of the sun, resulting in a darkening of the sky and a lowering of the temperature induces an increased activity. 3. Rainfall induces as a result of the rising moisture content of the marshes an increase of the activity in the direction of the nests, causing a decrease of the density on the marsh. 4. The animals hide in the nests during unfavourable weather conditions.
The Collembola of Cold Spring Beach, with special reference to the movements of the Poduridae
- C B Davenport
Davenport, C. B., 1903. The Collembola of Cold Spring Beach, with special reference to the movements of the Poduridae. Cold Spring Harbor Monographs 2: 3–32
Anurida maritima: an important sea-shore scavenger
- R W Dexter
Dexter, R. W., 1943. Anurida maritima: an important sea-shore scavenger. Journal of Economic Entomology 36: 797
- A D Imms
Imms, A. D., 1906. Anurida. Liverpool Marine Biology Committee,
XIII. Williams & Norgate, London.
Littoral apterygotes (Collembola and Thysanura)
- E N G Joosse
Joosse, E. N. G., 1976. Littoral apterygotes (Collembola and
Thysanura). In: L. Cheng (ed), Marine Insects. North-Holland
Publishing Company, Amsterdam, pp. 151–186.