Editing Diapause

{{short description|Response delay in animal dormancy}}
{{Dormancy}}
In animal [[dormancy]], '''diapause''' is the delay in development in response to regular and recurring periods of adverse environmental conditions.<ref>The Insects; Structure and Function, 4th Edition. R.F. Chapman, Cambridge University Press, 1998. {{ISBN|0-521-57048-4}}, p 403.</ref><ref name="Tauber">Tauber, M.J., Tauber, C.A., Masaki, S. (1986) ''Seasonal Adaptations of Insects''. Oxford University Press{{page needed|date=August 2020}}</ref> It is a [[physiological]] state with very specific initiating and inhibiting conditions. The mechanism is a means of surviving predictable, unfavorable environmental conditions, such as temperature extremes, drought, or reduced food availability. Diapause is observed in all the life stages of [[arthropod]]s, especially [[insect]]s. 

Activity levels of diapausing stages can vary considerably among species. Diapause may occur in a completely immobile stage, such as the [[pupae]] and eggs, or it may occur in very active stages that undergo extensive migrations, such as the adult [[monarch butterfly]], ''Danaus plexippus''. In cases where the insect remains active, feeding is reduced and reproductive development is slowed or halted.

[[Embryonic diapause]], a somewhat similar phenomenon, occurs in over 130 species of mammals, possibly even in humans,<ref>{{Cite journal |last1=Fenelon |first1=Jane C.|last2=Renfree |first2=Marilyn B.|date=2017-09-15 |title=The enigma of embryonic diapause |journal=Development |volume=144 |issue=18 |pages=3199–3210 |doi=10.1242/dev.148213 |issn=1477-9129 |pmid=28928280 |doi-access=free}}</ref><ref>{{Cite journal |last=Mohl |first=D |date=1997-03-07 |title=mTOR activity paces human blastocyst stage developmental progression |url=http://dx.doi.org/10.1016/s0092-8674(00)91910-x |journal=Cell |volume=88 |issue=5 |pages=675–684 |doi=10.1016/s0092-8674(00)91910-x |doi-broken-date=2024-11-18 |issn=0092-8674|url-access=subscription }}</ref> and in the [[embryo]]s of many of the [[oviparity|oviparous]] [[species]] of fish in the order [[Cyprinodontiformes]].<ref>{{cite journal |pmid=9254916 |title=A molecular phylogeny for aplocheiloid fishes (Atherinomorpha, Cyprinodontiformes): the role of vicariance and the origins of annualism |author=Glen E. Collier |author2=William J. Murphy |date= August 1997 |quote=Annual aplocheiloid killifish embryos possess a rare ability among vertebrates to enter stages of developmental arrest (diapause) when subjected to adverse environmental conditions. |volume=14 |issue=8 |journal=Mol. Biol. Evol. |pages=790–9 |doi=10.1093/oxfordjournals.molbev.a025819|doi-access=free }}</ref>

==Phases of insect diapause==
Diapause in insects is a dynamic process consisting of several distinct phases. While diapause varies considerably from one [[taxon]] of insects to another, these phases can be characterized by particular sets of metabolic processes and responsiveness of the insect to certain environmental stimuli.<ref name="Kostal">{{cite journal |last1= Kostal |first1= V |year= 2006 |title= Eco-physiological phases of insect diapause |journal= Journal of Insect Physiology |volume= 52 |issue= 2|pages= 113–127 |doi=10.1016/j.jinsphys.2005.09.008 |pmid=16332347|bibcode= 2006JInsP..52..113K }}</ref> For example, ''[[Sepsis cynipsea]]'' flies primarily use temperature to determine when to enter diapause.<ref>Blanckenhorn, W. U. (1998). Altitudinal differentiation in the diapause response of two species of dung flies. Ecological Entomology 23, 1-8.</ref> Similarly, ''[[Chrysoperla plorabunda]]'' lacewings regulate their reproductive cycle using daylight length, with adults entering reproductive diapause when there are less than 12-13 hours of daylight.<ref>{{Cite journal |last1=Tauber |first1=Catherine A. |last2=Tauber |first2=Maurice J. |date=June 1987 |title=Inheritance of seasonal cycles in Chrysoperla (Insecta: Neuroptera) |journal=Genetics Research |language=en |volume=49 |issue=3 |pages=215–223 |doi=10.1017/S0016672300027105 |issn=0016-6723|doi-access=free }}</ref> Diapause can occur during any stage of development in arthropods, but each species exhibits diapause in specific phases of development. Reduced oxygen consumption is typical as is reduced movement and feeding.<ref>The Insects; Structure and Function, 4th Edition. R.F. Chapman, Cambridge University Press, 1998. {{ISBN|0-521-57048-4}}, pp. 403–404</ref> In ''[[Polistes exclamans]]'', a social wasp, only the queen is said to be able to undergo diapause.<ref>{{cite journal |last1= Bohm |year= 1972 |title= Effects of environment and juvenile hormone on ovaries of the wasp, Polistes metricus |journal= Insect Physiology |volume= 18 |issue= 1 |pages= 1875–1883 |doi= 10.1016/0022-1910(72)90158-8|bibcode= 1972JInsP..18.1875B }}</ref>

===Comparison of diapause periods===
The sensitive stage is the period when stimulus must occur to trigger diapause in the organism. Examples of sensitive stage/diapause periods in various insects:<ref name=Chapman404>The Insects; Structure and Function, 4th Edition. R.F. Chapman, Cambridge University Press, 1998. {{ISBN|0-521-57048-4}}, p 404.</ref><br/>
{| class="wikitable"
|-
| '''Scientific name''' || '''Common name''' || '''Sensitive stage''' || '''Diapause'''
|-
|''[[Southwestern corn borer|Diatraea grandiosella]]'' || Southwestern corn borer || early larval || late larval<ref>Bulletin of Entomological Research (1976), 66:75–79 Cambridge University Press, Copyright © Cambridge University Press 1976, Diapause of the southwestern corn borer, ''Diatraea grandiosella'' Dyar (Lepidoptera, Pyralidae): effects of a juvenile hormone mimic: G. M. Chippendalea1 and C.-M. Yina1a1, Department of Entomology, University of Missouri, Columbia, Missouri 65201, U.S.A.</ref>
|-
|''[[Sarcophaga crassipalpis]]'' || Flesh fly || early larval || pupa
|-
|''[[Sarcophaga argyrostoma]]'' || Flesh fly || mid to late larval || pupa
|-
|''[[Manduca sexta]]'' || Tobacco hornworm || late embryonic (egg) to late larval || pupa
|-
|''[[Colorado beetle|Leptinotarsa decemlineata]]'' || Colorado potato beetle || early adult || late adult
|-
|''[[Bombyx mori]]'' || Silkworm || late embryonic (egg) to early larval || embryonic
|-
|''[[Gypsy moth|Lymantria dispar]]'' || Spongy moth || late embryonic || late embryonic
|-
|''[[Monarch (butterfly)|Danaus plexippus]]'' || Monarch butterfly || early adulthood || adulthood
|-
|''[[Acronicta rumicis]]''
|Knott grass moth
|mid larval
|mid larval
|-
|''[[Codling moth|Cydia pomonella]]''
|Codling moth
|early to mid larval 
|mid larval<ref>{{Cite book|title=The Biology of the Codling Moth as the Basis for Its Control|last=Tadic|first=M.|publisher=Univerzitet U Beogradu|year=1957}}</ref>
|-
|''[[Gynaephora groenlandica]]''
|Arctic woolly bear moth
|mid larval
|mid larval<ref>Makarova, O. L.; Sviridov, A. V.; Klepikov, M. A. (2013-04-01). "Lepidoptera (Insecta) of polar deserts". Entomological Review. 93 (2): 225–239.{{doi|10.1134/S0013873813020115}}. [[International Standard Serial Number|ISSN]] 0013-8738.</ref>
|-
|''[[Cuterebra fontinella]]'' || Mouse botfly || mid larval || pupa<ref>
{{cite journal |vauthors=Scholl PJ|title=Gonotrophic Development in the Rodent Bot Fly ''Cuterebra fontinella'' (Diptera: Oestridae)|journal=Journal of Medical Entomology|volume=28|issue=3|pages=474–476|year=1991|doi=10.1093/jmedent/28.3.474|pmid=1875379}}</ref>
|-
|''[[Nothobranchius furzeri]]
|turquoise killifish
|egg
|egg
|}

===Induction===
The induction phase occurs at a genetically predetermined stage of life, and occurs well in advance of the environmental stress.<ref name="Kostal" /> This sensitive stage may occur within the lifetime of the diapausing individual, or in preceding generations, particularly in egg diapause.<ref name="Huffaker">Huffaker, C.B. and Gutierrez, A.P., Eds. 1999. Ecological Entomology. John Wiley & Sons, Inc.</ref> During this phase, insects are responsive to external cues called token stimuli, which trigger the switch from direct development pathways to diapause pathways. Token stimuli can consist of changes in [[photoperiod]], [[thermoperiod]], or [[allelochemicals]] from food plants. These stimuli are not in themselves favourable or unfavourable to development, but they herald an impending change in environmental conditions.<ref name="Tauber" />

===Preparation===
The preparation phase usually follows the induction phase, though insects may go directly from induction to initiation without a preparation phase.<ref name="Kostal" /> During this phase, insects accumulate and store molecules such as [[lipids]], [[proteins]], and [[carbohydrates]]. These molecules are used to maintain the insect throughout diapause and to provide fuel for development following diapause termination. Composition of the [[cuticle]] may be altered by changing [[hydrocarbon]] composition and by adding [[lipids]] to reduce water loss, making the organism resistant to desiccation.<ref>{{cite journal |last1= HEGDEKAR |first1= B. M. |year= 1979 |title= Epicuticular Wax Secretion in Diapause and Non-diapause Pupae of the Bertha Army worm |journal= Annals of the Entomological Society of America |volume= 72 |issue= 1 |pages= 13–15|doi= 10.1093/aesa/72.1.13 }}</ref> Diapausing [[pupa]]ria of the [[flesh fly]], ''Sarcophaga crassipalpis'', increase the amount of cuticular [[hydrocarbons]] lining the puparium, effectively reducing the ability of water to cross the cuticle.<ref>{{cite journal |last1= Yoder |first1= J.A. |last2= Denlinger |first2= D.L. |last3= Dennis |first3= M.W. |last4= Kolattukudey |first4= P.E. |year= 1992 |title= Enhancement of diapausing flesh fly puparia with additional hydrocarbons and evidence for alkane biosynthesis by a decarbonylation mechanism |journal= Insect Biochemistry and Molecular Biology |volume= 22 |issue= 3 |pages= 237–243 |doi=10.1016/0965-1748(92)90060-r|bibcode= 1992IBMB...22..237Y }}</ref>

===Initiation===
[[Photoperiod]] is the most important stimulus initiating diapause.<ref name=Chapman404/> The initiation phase begins when morphological development ceases.<ref name="Kostal" /> In some cases, this change may be very distinct and can involve [[ecdysis|moulting]] into a specific diapause stage, or be accompanied by color change. [[Enzyme|Enzymatic]] changes may take place in preparation for [[cold hardening]]. For example, only diapausing adults of the fire bug, ''Pyrrhocoris apterus'', have the enzymatic complement that allows them to accumulate [[polyol|polyhydric alcohols]], molecules that help to lower their freezing points and thus avoid freezing.<ref>{{cite journal |last1= Kostal |first1= V. |last2= Tollarova |first2= M. |last3= Sula |first3= J. |year= 2004 |title= Adjustments of the enzymatic complement for polyol biosynthesis and accumulation in diapausing cold-acclimated adults of Pyrrhocoris apterus |journal= Journal of Insect Physiology |volume= 50 |issue= 4|pages= 303–313 |doi=10.1016/j.jinsphys.2004.01.006|pmid= 15081823 |bibcode= 2004JInsP..50..303K }}</ref> Insects may also undergo behavioural changes and begin to aggregate, [[insect migration|migrate]], or search for suitable [[overwinter]]ing sites.[[File:Angangueo monarchs.jpg|thumb|Overwintering [[monarch butterflies]] in diapause clustering on [[oyamel]] trees. One tree is completely covered in butterflies. These butterflies were located on a preserve outside of [[Angangueo]], [[Michoacán]], [[Mexico]]]]

===Maintenance===
During the maintenance phase, insects experience lowered [[metabolism]] and developmental arrest is maintained.<ref name="Kostal" /> Sensitivity to certain stimuli which act to prevent termination of diapause, such as photoperiod and [[temperature]], is increased. At this stage, insects are unresponsive to changes in the [[natural environment|environment]] that will eventually trigger the end of diapause, but they grow more sensitive to these stimuli as time progresses.

===Termination===
In insects that undergo obligate diapause, termination may occur spontaneously, without any external stimuli.<ref name="Kostal" /> In facultative diapausers, token [[stimulus (physiology)|stimuli]] must occur to terminate diapause. These [[stimulus (physiology)|stimuli]] may include chilling, freezing, or contact with [[water]], depending on the environmental conditions being avoided. These stimuli are important in preventing the insect from terminating diapause too soon, for instance in response to warm weather in late fall. In the [[Edith's checkerspot]] butterfly, individuals must receive enough sunlight in order to terminate the diapause stage and become a fully grown butterfly.<ref name="ten">{{cite journal |last1=Weiss |first1=Stuart B. |last2=White |first2=Raymond R. |last3=Murphy |first3=Dennis D. |last4=Ehrlich |first4=Paul R. |title=Growth and Dispersal of Larvae of Checkerspot Butterfly Euphydryas editha |journal=Oikos |date=October 1987 |volume=50 |issue=2 |pages=161–166 |doi=10.2307/3565996 |jstor=3565996|bibcode=1987Oikos..50..161W }}</ref> Termination may occur at the height of unfavourable conditions, such as in the middle of winter. Over time, depth of diapause slowly decreases until direct development can resume, if conditions are favourable. Termination can also occur in specific time frames linked to reproductive periods, such as in the beetle ''[[Colaphellus bowringi]]:'' diapause ends for spring-reproducing beetles between late February and early April and for autumn-reproducing beetles between mid August and early October''.''<ref>{{Cite journal |last1=Xue |first1=Fang-Sen |last2=Li |first2=Ai-Qing |last3=Zhu |first3=Xing-Fen |last4=Gui |first4=Ai-Li |last5=Jiang |first5=Pei-Lan |last6=Liu |first6=Xiao-Fen |date=August 20, 2002 |title=Diversity in life history of the leaf beetle, Colaphellus bowringi Baly |url=https://www.sciengine.com/AESK/doi/10.16380/j.kcxb.2002.45.4.494498;JSESSIONID=737db758-13f2-4432-a9aa-1297abd9b7ed |journal=Acta Entomologica Sinica |volume=45 |issue=4 |pages=494–498|doi=10.16380/j.kcxb.2002.45.4.494498 |doi-broken-date=1 November 2024 }}</ref>

===Post-diapause quiescence===
Diapause frequently ends prior to the end of unfavourable conditions and is followed by a state of [[wikt:quiescence|quiescence]] from which the insect can arouse and begin direct development, should conditions change to become more favourable.<ref name="Kostal" /> This allows the insect to continue to withstand harsh conditions while being ready to take advantage of good conditions as soon as possible.

==Regulation==
Diapause in insects is regulated at several levels. Environmental stimuli interact with genetic pre-programming to affect [[neuron]]al signalling, [[endocrine]] pathways, and, eventually, metabolic and enzymatic changes.

===Environmental===
Environmental regulators of diapause generally display a characteristic [[season|seasonal pattern]]. In [[temperate]] regions, photoperiod is the most reliable cues of seasonal change.<ref name="Huffaker" /> This informs entry into reproductive diapause for many northern insects, including the fruit fly ''[[Drosophila montana]].''<ref>{{Cite journal|last1=Salminen|first1=T. S.|last2=Vesala|first2=L.|last3=Hoikkala|first3=A.|date=2012-12-01|title=Photoperiodic regulation of life-history traits before and after eclosion: Egg-to-adult development time, juvenile body mass and reproductive diapause in ''Drosophila montana''|journal=Journal of Insect Physiology|volume=58|issue=12|pages=1541–1547|doi=10.1016/j.jinsphys.2012.09.007|pmid=23026647|bibcode=2012JInsP..58.1541S |issn=0022-1910}}</ref> Depending on the season in which diapause occurs, either short or long days can act as token stimuli. Insects may also respond to changing day length as well as relative day length. Temperature may also act as a regulating factor, either by inducing diapause or, more commonly, by modifying the response of the insect to photoperiod.<ref name="Huffaker" /> Insects may respond to thermoperiod, the daily fluctuations of warm and cold that correspond with night and day, as well as to absolute or cumulative temperature. This has been observed in many moth species including the [[Indian mealmoth]], where individuals diapause in different developmental stages due to environmental temperature.<ref>{{Cite journal|last=Tzanakakis|first=M. E.|date=1959-11-01|title=An ecological study of the Indian-meal mothPlodia interpunctella(Hübner) with emphasis on diapause|journal=Hilgardia|language=en|volume=29|issue=5|pages=205–246|doi=10.3733/hilg.v29n05p205|issn=0073-2230|doi-access=free}}</ref> Food availability and quality may also help regulate diapause. In the [[desert locust]], ''Schistocerca gregaria'', a plant [[hormone]] called [[gibberellin]] stimulates [[reproduction|reproductive]] development.<ref>{{cite journal |last1= Ellis |first1= P.E. |last2= Carlisle |first2= D.B. |last3= Osborne |first3= D.J. |year= 1965 |title= Desert locusts: sexual maturation delayed by feeding on senescent vegetation |journal= Science |volume= 149 |issue= 3683 |pages= 546–547 |doi=10.1126/science.149.3683.546 |pmid=17843190|bibcode= 1965Sci...149..546E |s2cid= 34321076 }}</ref> During the dry season, when their food plants are in [[senescence]] and lacking gibberellin, the locusts remain immature and their reproductive tracts do not develop.

===Neuroendocrine===
The [[neuroendocrinology|neuroendocrine]] system of insects consists primarily of neurosecretory cells in the [[brain]], the corpora cardiaca, corpora allata and the prothoracic glands.<ref name="Tauber" /> There are several key [[hormone]]s involved in the regulation of diapause: [[juvenile hormone]] (JH), diapause hormone (DH), and [[prothoracicotropic hormone|prothoracicotropic hormone (PTTH)]].<ref name="Denlinger">{{cite journal |last1= Denlinger |first1= D.L. |year= 2002 |title= Regulation of diapause |journal= Annual Review of Entomology |volume= 47 |pages= 93–122 |doi= 10.1146/annurev.ento.47.091201.145137|pmid= 11729070 }}</ref>

Prothoracicotropic hormone stimulates the prothoracic glands to produce [[ecdysteroids]] that are required to promote development.<ref name="Denlinger" /> Larval and pupal diapauses are often regulated by an interruption of this connection, either by preventing release of prothoracicotropic hormone from the brain or by failure of the prothoracic glands to respond to prothoracicotropic hormone.

The corpora allata is responsible for the production of [[juvenile hormone]] (JH). In the bean bug, ''Riptortus pedestris'', clusters of [[neurons]] on the [[protocerebrum]] called the [[pars lateralis]] maintain reproductive diapause by inhibiting JH production by the [[corpora allata]].<ref>{{cite journal |last1= Shimokawa |first1= K. |last2= Numata |first2= H. |last3= Shiga |first3= S. |year= 2008 |title= Neurons important for the photoperiodic control of diapause in the bean bug, ''Riptortus pedestris'' |journal= Journal of Comparative Physiology |volume= 194 |issue= 8|pages= 751–762 |doi=10.1007/s00359-008-0346-y|pmid= 18546002 |s2cid= 28631269 }}</ref> Adult diapause is often associated with the absence of JH, while larval diapause is often associated with its presence.

In adults, absence of JH causes degeneration of flight [[muscles]] and [[atrophy]] or cessation of development of reproductive tissues, and halts mating behaviour. The presence of JH in larvae may prevent moulting to the next larval [[instar]], though successive stationary moults may still occur.<ref>{{cite journal |last1= Yin |first1= C.M. |last2= Chippendale |first2= G.M. |year= 1979 |title= Diapause of the Southwestern Corn Borer, ''Diatraea grandiosella'': further evidence showing juvenile hormone to be the regulator |journal= Journal of Insect Physiology |volume= 25 |issue= 6|pages= 513–523 |doi=10.1016/s0022-1910(79)80010-4|bibcode= 1979JInsP..25..513Y }}</ref> In the corn borer, ''Diatraea gradiosella'', JH is required for the accumulation by the fat body of a storage [[protein]] that is associated with diapause.<ref>{{cite journal |last1= Brown |first1= J.J. |last2= Chippendale |first2= G.M. |year= 1978 |title= Juvenile hormone and a protein associated with the larval diapause of the Southwestern Corn Borer, ''Diatraea grandiosella'' |journal= Insect Biochemistry |volume= 8 |issue= 5|pages= 359–397 |doi=10.1016/0020-1790(78)90022-7}}</ref>

Diapause hormone regulates [[embryo]]nic diapause in the eggs of the [[silkworm]] moth, ''Bombyx mori''.<ref>{{cite journal |last1= Horie |first1= Y. |last2= Kanda |first2= T. |last3= Mochida |first3= Y. |year= 2000 |title= Sorbitol as an arrester of embryonic development in diapausing eggs of the silkworm, ''Bombyx mori'' |journal= Journal of Insect Physiology |volume= 46 |issue= 6|pages= 1009–1016 |doi=10.1016/s0022-1910(99)00212-7|pmid= 10802114 |bibcode= 2000JInsP..46.1009H }}</ref> DH is released from the [[subesophageal ganglion]] of the mother and triggers [[trehalase]] production by the [[ovaries]]. This generates high levels of [[glycogen]] in the [[egg (biology)|eggs]], which is converted into the polyhydric alcohols [[glycerol]] and sorbitol. [[Sorbitol]] directly inhibits the development of the embryos. [[Glycerol]] and [[sorbitol]] are reconverted into [[glycogen]] at the termination of diapause.

==Tropical diapause==
Diapause in the [[tropics]] is often initiated in response to [[biotic component|biotic]] rather than [[abiotic component]]s.<ref name="DenlingerD">{{cite journal |last1= Denlinger |first1= D.L. |year= 1986 |title= Dormancy in tropical insects |journal= Annual Review of Entomology |volume= 31 |pages= 239–264 |doi=10.1146/annurev.en.31.010186.001323 |pmid=3510585}}</ref> For example, food in the form of [[vertebrate]] carcasses may be more abundant following dry seasons, or [[oviposition]] sites in the form of fallen [[trees]] may be more available following rainy seasons. Also, diapause may serve to synchronize mating seasons or reduce competition, rather than to avoid unfavourable climatic conditions.

Diapause in the tropics poses several challenges to insects that are not faced in [[temperate]] zones.<ref name="DenlingerD" /> Insects must reduce their metabolism without the aid of cold temperatures and may be faced with increased water loss due to high temperatures. While cold temperatures inhibit the growth of [[fungi]] and [[bacteria]], diapausing tropical insects still have to deal with these [[pathogens]]. Also, [[predation|predator]]s and [[parasitism|parasites]] may still be abundant during the diapause period.

Aggregations are common among diapausing tropical insects, especially in the orders [[Coleoptera]], [[Lepidoptera]], and [[Hemiptera]].<ref name="DenlingerD" /> Aggregations may be used as protection against [[predation]], since aggregating species are frequently toxic and predators quickly learn to avoid them. They can also serve to reduce water loss, as seen in the fungus [[beetle]], ''[[Stenotarsus]] rotundus'', which forms aggregations of up to 70,000 individuals, which may be eight beetles deep. [[Relative humidity]] is increased within the aggregations and beetles experience less water loss, probably due to decreased surface area to volume ratios reducing evaporative water loss.<ref>{{cite journal |last1= Yoder |first1= J.A. |last2= Denlinger |first2= D.L. |last3= Wolda |first3= H. |author-link3=Henk Wolda |year= 1992 |title= Aggregation promotes water conservation during diapause in the tropical fungus beetle, ''Stenotarsus rotundus'' |journal= Entomologia Experimentalis et Applicata |volume= 63 |issue= 2|pages= 203–205 |doi=10.1111/j.1570-7458.1992.tb01574.x|bibcode= 1992EEApp..63..203Y |s2cid= 84347660 }}</ref>

==See also==
[[Embryonic diapause]]
*''[[Eburia quadrigeminata]]'', the species with the longest reported diapause among insects (up to 40 years).
*''[[Polygonia c-album]]'', whose larvae exhibit density-dependent polymorphism where one of two morphs is a diapausing phase.
*''[[Nebria brevicollis]],'' a carabid beetle who exhibits diapause behavior due to low food resource availability. 

==References==
{{reflist}}

[[Category:Physiology]]
[[Category:Developmental biology]]
[[Category:Ethology]]
[[Category:Animal migration]]
[[Category:Arthropod ecology]]
[[Category:Lepidopterology]]