This article was downloaded by: [Temple University Libraries]On: 15 November 2014, At: 18:27Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Biological Rhythm ResearchPublication details, including instructions for authors andsubscription information:http://www.tandfonline.com/loi/nbrr20

Circadian Patterns of Migration ofStrinatia brevipennis (Orthoptera:Phalangopsidae) inside a CaveS. Hoenen & M.D. MarquesPublished online: 09 Aug 2010.

To cite this article: S. Hoenen & M.D. Marques (1998) Circadian Patterns of Migrationof Strinatia brevipennis (Orthoptera: Phalangopsidae) inside a Cave, Biological RhythmResearch, 29:5, 480-487, DOI: 10.1076/brhm.29.5.480.4826

To link to this article: http://dx.doi.org/10.1076/brhm.29.5.480.4826

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information(the “Content”) contained in the publications on our platform. However, Taylor& Francis, our agents, and our licensors make no representations or warrantieswhatsoever as to the accuracy, completeness, or suitability for any purposeof the Content. Any opinions and views expressed in this publication are theopinions and views of the authors, and are not the views of or endorsed byTaylor & Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information. Taylor andFrancis shall not be liable for any losses, actions, claims, proceedings, demands,costs, expenses, damages, and other liabilities whatsoever or howsoever causedarising directly or indirectly in connection with, in relation to or arising out of theuse of the Content.

This article may be used for research, teaching, and private study purposes.Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly

forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014

Biological Rhythm Research, 1998, Vol. 29, No. 5, pp. 480–487 0929-1016/98/2905-0480$12.00© Swets & Zeitlinger

Circadian Patterns of Migration ofStrinatia brevipennis (Orthoptera: Phalangopsidae)

inside a Cave

S. Hoenen and M.D. Marques

Museu de Zoologia, University of S.Paulo, S.Paulo, Brazil

ABSTRACT

The distribution pattern of a population of the cricket Strinatia brevipennis was studied in a cave inSoutheastern Brazil. The individuals do not move very often, but the population, as a whole, changesposition along the day and night. Although the crickets never leave the cave, they approach theentrance during the night for feeding. During the day, they return to the deep regions and remainalmost motionless. The migration seems to be related to light intensity but not to temperature orrelative humidity. A photophobic response is slightly evident but the possibility of the presence of anendogenous control of both, sensitivity to light and activity, must also be considered.

KEYWORDS: Orthoptera, cricket, cave, circadian rhythm, locomotion.

INTRODUCTION

Against the generally accepted idea of stability of the cave climate, cave organ-isms are subjected to daily environmental variations, either strong or slight (Hus-son, 1971). These variations are observed as daily and annual cycles of relativehumidity and temperature that are detected even at the deep regions. These condi-tions may vary from one cave to the other in accordance with their topography(vertically or horizontally oriented caves), dimensions, internal morphology,number of entrances, etc. Air flow and winds regimen established by these phys-ical features, combined with variations of the external weather determine theclimatic pattern of caves (Racovitza, 1975). More accentuated environmentaloscillations, including light/dark cycles, are detected at the proximate regions anddecrease according to a gradient until the intermediate zones of some caves whichhave a more exposed entrance.

Address correspondence to: Museu de Zoologia USP, Caixa Postal 42694, 04299-970 S. Paulo, SP,Brazil. Phonefax (5511) 274-3455; 274-3690; e-mail: smhoenen@usp.br

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014

481CIRCADIAN MIGRATION PATTERNS OF STRINATIA BREVIPENNIS

Animals living in cave habitats may present rather different degrees of relationto the surface, according to the species (Holsinger & Culver, 1988), from thespecies that periodically leave the caves, to those that inhabit only the subterrane-an environment. Circadian rhythmicity has already been detected in some caveinsects (Saunders, 1982) and it is probably important to those which return to thesurface, providing the fine time adjustment of exits and returns to the cave. As forthe ones that permanently live in the caves, it is generally accepted that theirclocks have been suppressed (Lamprecht & Weber, 1991). Nevertheless, as cycles(even attenuated ones) are present in some caves, it is possible that some rhythmiccharacteristics persist. However, as the studies are so few, evidences are stilllacking.

Several cricket species are known as cave inhabitants and show different adap-tive strategies to the environment. Strinatia brevipennis is a nocturnal, non sing-ing cricket, living in caves in Southeastern Brazil. This species has no gregarioushabits and the small populations of about 10 to 15 individuals observed in eachcave do not show interactions among them (S.Hoenen, unpubl. obs.).

In this study, a population of S. brevipennis has been observed following achronobiological protocol, carefully avoiding a direct intervention by the observ-er or the use of instruments that could introduce deviations in a cavernicolous’behaviour. The objective was to register activity and behavioural items, and totrace an eventual influence of the oscillations of environmental variables.

MATERIAL AND METHODS

The cave chosen was Gruta da Mãozinha (24°16′10′′S; 48°26′55′′W) at the ParqueEstadual Intervales, São Paulo, Brazil.

An average of 10 crickets was observed each four hours, with 3 minutes ofobservation per cricket. Observations were made during three consecutive days,under red light (680 nm). The observations consisted in the measurement of thedistance between each animal and a fixed point at the entrance. Temperature andrelative humidity were measured on the spot where each cricket was observed. Asfor light intensity, the photometer did not measure indirect light, which is the onlyform of light available at the entrance of the cave. Being so, the position of eachcricket was registered as being in the photic or aphotic region, during the light ordark phase.

Behavioural items observed were classified in the categories: motionless, per-forming grooming, walking and running.

Circadian periodicities were tested using the COSINOR test method (modifiedby Benedito-Silva, 1997). The dependence of some variable in relation to otherswas tested by regression analyses (Zar, 1996).

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014

482 S. HOENEN AND M.D. MARQUES

RESULTS

The cave studied is located at a mountainous region with altitudes ranging from70 to 1000 m and in a climate temperate humid without a dry season (Setzer,1966), temperature varying from 17 to 19°C. The cave consists basically of a duct54 m long with two great halls: one intermediate, with a little opening at theceiling, and another distal and dark (see Gnaspini-Netto & Trajano, 1992). Thephotic (illuminated) region in this cave goes until 6 m from the actual entranceand in this study all of this region is considered as ‘entrance’, in contrast with thefollowing part which is the ‘deep region’.

The crickets have been seen in the walls, mainly near to the ground. In eachinspection, around 12 crickets were found, dispersed from the entrance until 15 mdeep, but this number varied along the day. Activity occurred mainly during thenight. Most adults and nymphs showed a migration towards the entrance neardusk, where they concentrate until dawn. Disturbances of the environment evokedstronger and faster reactions (e.g. running away) when they occurred after 1700 hand during the night than during the day. No other behaviour besides locomotionwas observed.

Temperature and relative humidity showed small oscillations (Fig.1). Howev-er, when data were analysed by the COSINOR method, the results (Table 1)showed valid daily cycles of temperature and relative humidity.

Most crickets remained motionless during the whole observation interval, witha few episodes of “running” and “walking” (data are summarized in Fig. 2 (top)).No statistically significant circadian rhythm was detected by the COSINOR anal-ysis.

Fig. 1. Temperature (◆) and relative humidity (/) variations along the day at the Mãozinha cave,São Paulo, Brazil. Mean values.

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014

483CIRCADIAN MIGRATION PATTERNS OF STRINATIA BREVIPENNIS

The population changed place along the 4 days. Chi-square tests have beenperformed to check eventual significant differences between the patterns of distri-bution of the population and of activity during the day (09:00 h, 13:00 h, 17:00 h)and the night (21:00 h, 01:00 h) for both the locomoting and motionless insects.As Table 2 shows, it was not possible to differentiate nocturnal from diurnalactivity, probably because the animals did not move very much. Differencesbecame evident when the number of motionless individuals near the entrance wascompared with that of those at the deep region, and the number of motionlessindividuals during the day compared with the same during the night. Consideringthe number of individuals at the first 6 m from the entrance, and excluding thedata of 05:00 h, because at this timepoint there was sunlight already, it was possi-ble to demonstrate (Table 2) that the crickets were significantly farther from theentrance during the day than during the night.

The distribution of all individuals inside the cave was mapped and grouped(Fig. 2 (bottom)) showing that crickets migrate inwards the cave during the dayuntil noon, returning to the entrance after sunset. This migration towards the deep

TABLE 1. COSINOR analysis of environmental temperature and relative humidity variations along24 h at the Mãozinha cave, S. Paulo State, Brazil.

Acrophase Amplitude Mesor p value

Temperature 19:43 h 0.71 19.33 < 0.001

Relative humidity 08:40 h 4.15 94.44 < 0.001

TABLE 2. Comparisons between the number of locomoting and motionless crickets at differemttimes of the day and in two localities: entrance and deep region, inside the Mãozinhacave, S. Paulo, Brazil. Chi-square analysis; X2 = values obtained; X2

0.05 = critical values;υ = degress of freedom.

X2 υ X20.05 p-value

Moving Cricketsnight X day 2.0 1 3.841 > 0.05entrance X deep 2.13 1 3.841 > 0.05

Non moving Cricketsnight X day 16.57 1 3.841 < 0.05entrance X deep 11.54 1 3.841 < 0.05

Distance until 6mnight X day 12.92 5 11.07 < 0.05

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014

484 S. HOENEN AND M.D. MARQUES

region occurs when in the entrance luminosity is intense, the temperature high,and relative humidity very low. The results of measured distances were treated bythe COSINOR test. Parameters obtained were: acrophase 13:09 h, amplitude 2.26,and Mesor 13.97 (p = 0.001), indicating that this migration may be a populationbehaviour with a circadian pattern.

Regression analyses of migration with temperature and relative humidity didnot show significant influence of neither (temperature: t value = 1.22, p = 0.2;relative humidity: t value = 0.91, p = 0.4). As the main displacements of theindividuals were observed at the photic zone, the analyses have been done em-ploying the number of animals found until 6 m inside the cave, related to temper-

Fig. 2. Activity parameters of S. brevipennis at each sampled hour. (top) Distribution of activitypatterns. Bars represent the percentage of individuals performing each activity parameter perhour. Grey = motionless; Black = walking; White = running. (bottom) Distances of eachcricket from the entrance (0 m) of the cave. Data from three days were grouped.

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014

485CIRCADIAN MIGRATION PATTERNS OF STRINATIA BREVIPENNIS

ature and relative humidity data collected over the same distance. Both interrela-tionships were not significant (temperature: t value = 0.257; p = 0.8; relativehumidity: t value = 0.121; p = 0.9).

Because the statistical tests failed to corroborate a possible influence of envi-ronmental cycles, the recurrence of migration suggests the presence of a circadiancomponent. In addition, as the population changes position each 4 h, as shown inFig. 2b, it is possible that an ultradian rhythm is present as well.

DISCUSSION

Nocturnal migrations outside caves were already observed for several cricketspecies: Hadenoecus subterraneus (Reichle, 1963), Ceuthophilus conicaudus(Campbell, 1976), Dolichopoda spp. and Troglophilus spp. (Husson, 1971). Had-enoecus subterraneus goes to the surface looking for food (Norton, 1978). How-ever, only one third of the population was seen leaving the cave each night (Park& Reichle, 1963). This species showed persistence of the locomotor rhythm underconstant darkness, with a peak in the middle of the subjective night (Reichle et al.,1965). As for Ceuthophilus conicaudus, its activity patterns have been correlatedwith several environmental factors and emergence from the cave occurred after20:00 h until 06:00 h (Campbell, 1976). For both species, starvation has beenconsidered as the signal for activity to start and oscillations of climatic conditions,mainly in the in deep regions, would play only a secondary role (Campbell, 1976;Reichle et al., 1965).

This may be the case in the present study. Strinatia brevipennis has never beenfound outside the cave but showed a nocturnal migration towards the entrance.This migration presented a circadian component, manifested as a population rhythmand starvation might be the signal for the process to start. Interestingly, individu-als did not show circadian rhythms, even though the immediate environmentshowed daily cycles of temperature and relative humidity.

The results presented here failed to detect any influence of either temperatureor relative humidity cycles on the population migration. This leaves the light/darkcycle as the most probable candidate for a zeitgeber. Very dim light, as the starlight (nearly 10–6 lux), is the synchronizer of the activity rhythms of cave beetles,according to Weber et al. (1994). Joshi and Chandrashekaran (1982) also showedsynchronization of locomotion rhythms of bats in light values of about 10–4 lux. Itseems that those species that live near entrances (or similar habitats) could presentstrong light sensibility, therefore even cycles of dim light and dark could act aseffective zeitgebers.

The migration observed in this study could be the expression of an endogenousrhythm or merely a direct response to the environment. The presence of an endog-

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014

486 S. HOENEN AND M.D. MARQUES

enous clock in crickets has been demonstrated by Tomioka and Chiba (1986) inGryllus bimaculatus. An endogenous circadian rhythm of the electroretinogram(Tomioka & Chiba, 1982) indicates a daily variation of the compound eye sensi-tivity to light and a mutual synchronization of the clocks bilaterally situated in themedullae. Whether or not this is the case for S. brevipennis is impossible to say,but this species has strongly pigmented eyes suggesting high sensitivity to light(S.Hoenen, unpublished observations; G. Fleissner, pers. commun.). Therefore,even if the migration observed is due to entrainment to the light/dark environmen-tal cycle, a photophobic reaction may be present, mediated or not by a circadianrhythm of the retinal responses.

As for the non-detection of circadian rhythms at the individual level, somespeculations could be advanced. Laboratory observations showed that these crick-ets have a poor behaviour repertoire and spend much time completely motionless.Notwithstanding these results, it may be that at the caves, the crickets can performother behavioural steps not seen in this study either because of the long intervalbetween two observations (3 h) or the short time each cricket was observed (3minutes). Even so, there are evidences that the adaptation to the cave environmententails certain peculiarities. What these characteristics are is difficult to ascertain,but the development of sensory structures to detect food and other individuals, forinstance, could give to the food availability or to the population the role of impor-tant zeitgebers. Intercourses between the individuals have not been observed, butthe ecological importance of the effect of the group cannot be discarded.

ACKNOWLEDGEMENTS

The authors are indebted to A.A. Benedito-Silva and J.M. Waterhouse for the many suggestions forstatistical analyses and also to P. Gnaspini for the revision and helpful suggestions to the manuscript.This study was supported by grants # 96/2494-3 (S.H.) and 92/4445-9 (M.D.M.) from FAPESP. Wealso thank Fundação Florestal do Estado de São Paulo which allowed visits and provided supportduring field studies in the caves.

REFERENCES

Benedito-Silva AA (1997): Aspectos metodológicos da cronobiologia. In: Marques N and Menna-Barreto L (eds.) Cronobiologia: Princípios e Aplicações. EDUSP, São Paulo, 215–238.

Cambell GD (1976): Activity rhythm in the cave cricket, Ceuthophilus conicaudus Hubbell. Am MidlNatur 96: 350–366.

Gnaspini-Netto P, Trajano E (1992): Província espeleológica do Vale do Ribeira, região da FazendaIntervales, S.P.: exploração, topografia e biologia. Espeleo-Tema 16: 41–74.

Holsinger JR, Culver DC (1988): The invertebrate cave fauna of Virginia and a part of EasternTennesse: Zoogeography and ecology. Brimleyana 14: 1–162.

Husson R (1971): Rythmes biologiques et vie cavernicole. Bull Soc Zool France 96, 3: 301–316.Joshi D, Chandrashekaran MK (1982): Daylight dimmer than starlight entrains the circadian rhythms

of a bat. Naturwissensch 69: 192–193.

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014

487CIRCADIAN MIGRATION PATTERNS OF STRINATIA BREVIPENNIS

Lamprecht G, Weber F (1991): Spontaneous locomotion behaviour in cavernicolous animals: theregression of the endogenous circadian system. In: CAMACHO, A.I. (ed.) The NaturalHistory of Biospeleology. Monografias del Museo Nacional de Ciencias Naturales, España,225–262.

Norton RM (1978): The biology of Hadenoecus subterraneus and Hadenoecus cumberladicus. In:Hubbell TH and Norton RM (eds.). The Systematics and Biology of the Cave Crickets ofthe American Tribe Hadenoecini (Orthoptera Saltatoria: Ensifera: Rhaphidophoridae: Doli-chopodinae). Misc Publ Mus Zool Univ Mich 156: 100–117.

Park O, Reichle D (1963): Observations on the ecology and behavior of the cave cricket, Hadenoecussubterraneus (Scudder). Bull Ecol Soc Am 44: 126–127.

Racovitza G (1975): La classification topoclimatique des cavités souterraines. Trav Inst Spéol EmileRacovitza (Bucarest), 14: 197–216.

Reichle DE (1963): Rhythmic activity in the cave cricket Hadenoecus subterraneus (Scudder). BullEcol Soc Am (abstr.) 44: 89.

Reichle DE, Palmer JD, Park O (1965): Persistent rhythmic locomotor activity in the cave cricket,Hadenoecus subterraneus, and its ecological significance. Am Midl Natur 74, 1: 57–66.

Saunders DS (1982): Insect Clocks. Pergamon Press, Oxford. 2nd.edition. 409p.Setzer J (1966): Atlas climático e ecológico do Estado de São Paulo. Comissão Interestadual da

Bacia Paraná-Uruguai, São Paulo. 61p.Tomioka K, Chiba Y (1982): Persistence of circadian ERG rhythm with optic tract severed. Natur-

wissensch 69: 355–356.Tomioka K, Chiba Y (1986): Circadian rhythm in the neurally isolated lamina-medulla complex in

the cricket, Gryllus bimaculatus. J Insect Physiol 35: 827–835.Weber F, Casale A, Lamprecht G, Rusdea E (1994): Highly sensitive reactions of microphthalmic

carabid beetles to light/dark cycles. In: Desender K et al. (eds). Carabid Beetles: Ecologyand Evolution. Kluwer Academic Publishers, Netherlands. 219–225.

Zar JH (1996): Biostatistical analysis. Prentice Hall, New Jersey. 407–445.

Dow

nloa

ded

by [

Tem

ple

Uni

vers

ity L

ibra

ries

] at

18:

27 1

5 N

ovem

ber

2014