From Aggregation to Dispersion: How Habitat Fragmentation Prevents the Emergence of Consensual Decision Making in a Group

In fragmented landscape, individuals have to cope with the fragmentation level in order to aggregate in the same patch and take advantage of group-living. Aggregation results from responses to environmental heterogeneities and/or positive influence of the presence of congeners. In this context, the fragmentation of resting sites highlights how individuals make a compromise between two individual preferences: (1) being aggregated with conspecifics and (2) having access to these resting sites. As in previous studies, when the carrying capacity of available resting sites is large enough to contain the entire group, a single aggregation site is collectively selected. In this study, we have uncoupled fragmentation and habitat loss: the population size and total surface of the resting sites are maintained at a constant value, an increase in fragmentation implies a decrease in the carrying capacity of each shelter. For our model organism, Blattella germanica, our experimental and theoretical approach shows that, for low fragmentation level, a single resting site is collectively selected. However, for higher level of fragmentation, individuals are randomly distributed between fragments and the total sheltered population decreases. In the latter case, social amplification process is not activated and consequently, consensual decision making cannot emerge and the distribution of individuals among sites is only driven by their individual propensity to find a site. This intimate relation between aggregation pattern and landscape patchiness described in our theoretical model is generic for several gregarious species. We expect that any group-living species showing the same structure of interactions should present the same type of dispersion-aggregation response to fragmentation regardless of their level of social complexity.

[1]  Zhen Wang,et al.  If players are sparse social dilemmas are too: Importance of percolation for evolution of cooperation , 2012, Scientific Reports.

[2]  Jean-Louis Deneubourg,et al.  Impact of increasing deployment of artificial floating objects on the spatial distribution of social fish species , 2013 .

[3]  C Rivault,et al.  Cuticular extracts inducing aggregation in the German cockroach, Blattella germanica (L.). , 1998, Journal of insect physiology.

[4]  Y. Sadovy,et al.  Reef Fish Spawning Aggregations: Biology, Research and Management , 2012, Fish & Fisheries Series.

[5]  Jean-Louis Deneubourg,et al.  Integration of an Autonomous Artificial Agent in an Insect Society: Experimental Validation , 2006, SAB.

[6]  T. Goldsmith,et al.  Spectral sensitivities of color receptors in the compound eye of the cockroach Periplaneta. , 1970, The Journal of experimental zoology.

[7]  Thierry Boulinier,et al.  The use of conspecific reproductive success for breeding patch selection in terrestrial migratory species , 1997, Evolutionary Ecology.

[8]  M. Dambach,et al.  Aggregation density and longevity correlate with humidity in first-instar nymphs of the cockroach (Blattella germanica L., Dictyoptera). , 1999, Journal of insect physiology.

[9]  Attila Szolnoki,et al.  Percolation threshold determines the optimal population density for public cooperation , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[10]  Charles M. Francis,et al.  Confronting collinearity: comparing methods for disentangling the effects of habitat loss and fragmentation , 2009, Landscape Ecology.

[11]  J. Deneubourg,et al.  Group Living Enhances Individual Resources Discrimination: The Use of Public Information by Cockroaches to Assess Shelter Quality , 2011, PloS one.

[12]  James T. Costa,et al.  The Other Insect Societies , 2006 .

[13]  F Mondada,et al.  Social Integration of Robots into Groups of Cockroaches to Control Self-Organized Choices , 2007, Science.

[14]  D J Meyer,et al.  The shadow response of the cockroach periplaneta americana. , 1981, Journal of neurobiology.

[15]  Robert J Fletcher,et al.  Emergent properties of conspecific attraction in fragmented landscapes. , 2006, The American naturalist.

[16]  M. Massot,et al.  CONSPECIFIC REPRODUCTIVE SUCCESS AND BREEDING HABITAT SELECTION: IMPLICATIONS FOR THE STUDY OF COLONIALITY , 1998 .

[17]  Jean-Louis Deneubourg,et al.  Collective Decision-Making Based on Individual Discrimination Capability in Pre-social Insects , 2006, SAB.

[18]  Claire Detrain,et al.  Self-amplification as a source of interindividual variability: shelter selection in cockroaches. , 2009, Journal of insect physiology.

[19]  José Halloy,et al.  Collegial decision making based on social amplification leads to optimal group formation. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[20]  C. Rivault,et al.  Food stealing in cockroaches , 1990, Journal of Ethology.

[21]  T. Valone,et al.  Public Information: From Nosy Neighbors to Cultural Evolution , 2004, Science.

[22]  W. Herrnkind,et al.  The guide effect influence on the gregariousness of juvenile Caribbean spiny lobsters , 2001, Animal Behaviour.

[23]  Thomas J Valone,et al.  Public information for the assessment of quality: a widespread social phenomenon. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  Romuald N. Lipcius,et al.  Shelter Selection by Spiny Lobster Under Variable Predation Risk, Social Conditions, and Shelter Size , 1992 .

[25]  T. Caraco,et al.  Social Foraging Theory , 2018 .

[26]  D. V. Vuren Ectoparasites, Fitness, and Social Behaviour of Yellow‐Bellied Marmots , 2010 .

[27]  J. Gascoigne,et al.  Allee Effects in Ecology and Conservation , 2008 .

[28]  M. Sunquist,et al.  The relative influence of habitat loss and fragmentation: do tropical mammals meet the temperate paradigm? , 2011, Ecological Applications.

[29]  W. C. Allee Animal Aggregations: A Study in General Sociology , 1931 .

[30]  A. Kacelnik,et al.  Foraging rate versus sociality in the starling Sturnus vulgaris , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[31]  Mathieu Lihoreau,et al.  Kin recognition via cuticular hydrocarbons shapes cockroach social life , 2009 .

[32]  W. C. Allee Animal aggregations, a study in general sociology. / by W. C. Allee. , 1931 .

[33]  J. Wiens Population Responses to Patchy Environments , 1976 .

[34]  J. Deneubourg,et al.  Dynamics of aggregation in Lasius niger (Formicidae): influence of polyethism , 2004, Insectes Sociaux.

[35]  V. Isaeva Self-organization in biological systems , 2012, Biology Bulletin.

[36]  I. Giardina Collective Animal Behavior David J.T. Sumpter Collective Animal Behavior , 2011, Animal Behaviour.

[37]  R. Clark,et al.  AVIAN HABITAT SELECTION: PATTERN FROM PROCESS IN NEST-SITE USE BY DUCKS? , 1999 .

[38]  Charles R. Brown,et al.  Coloniality in the Cliff Swallow: The Effect of Group Size on Social Behavior , 1996 .

[39]  E. Danchin,et al.  The evolution of coloniality: the emergence of new perspectives. , 1997, Trends in ecology & evolution.

[40]  L. Fahrig Effects of Habitat Fragmentation on Biodiversity , 2003 .

[41]  R. R. Krausz Living in Groups , 2013 .

[42]  K. L. Muller The role of conspecifics in habitat settlement in a territorial grasshopper , 1998, Animal Behaviour.

[43]  J. Hutchinson Animal groups in three dimensions , 1999 .

[44]  J. Clobert,et al.  Availability and use of public information and conspecific density for settlement decisions in the collared flycatcher , 2004 .

[45]  Stephens,et al.  Consequences of the Allee effect for behaviour, ecology and conservation. , 1999, Trends in ecology & evolution.

[46]  J. Deneubourg,et al.  Self-organized aggregation in cockroaches , 2005, Animal Behaviour.

[47]  A. Møller,et al.  Cuckoldry and Sociality: A Comparative Study of Birds , 1993, The American Naturalist.

[48]  G. Fraenkel,et al.  The Orientation of Animals, Kineses, Taxes and Compass Reactions, , 1941 .

[49]  Jean-Louis Deneubourg,et al.  Complex dynamics based on a quorum: decision-making process by cockroaches in a patchy environment. , 2009 .

[50]  W. Hamilton Geometry for the selfish herd. , 1971, Journal of theoretical biology.

[51]  J. Deneubourg,et al.  Cockroach aggregation based on strain odour recognition , 2004, Animal Behaviour.

[52]  M. Thiel,et al.  Chemical communication in crustaceans , 2011 .

[53]  O. Rueppell,et al.  A review on self-destructive defense behaviors in social insects , 2012, Insectes Sociaux.

[54]  J. Deneubourg,et al.  Conspecific Attraction and Shelter Selection in Gregarious Insects , 2007, The American Naturalist.

[55]  J. Deneubourg,et al.  Does social behavior influence the dynamics of aggregations formed by tropical tunas around floating objects ? An experimental approach , 2013 .

[56]  Colette Rivault,et al.  Cuticular hydrocarbon profiles and aggregation in four Periplaneta species (Insecta: Dictyoptera). , 2005, Journal of insect physiology.

[57]  V. V. Krishnan,et al.  NONINTUITIVE CUE USE IN HABITAT SELECTION , 2005 .

[58]  Edward Osborne Wilson,et al.  Cockroaches: Ecology, Behavior, and Natural History , 2007 .

[59]  M. Lihoreau,et al.  The social biology of domiciliary cockroaches: colony structure, kin recognition and collective decisions , 2012, Insectes Sociaux.

[60]  Sebastian Santiago,et al.  Ideal Free Distribution , 2007 .

[61]  Lenore Fahrig,et al.  Response of predators to loss and fragmentation of prey habitat: a review of theory. , 2006, Ecology.

[62]  L. Edelstein-Keshet,et al.  Complexity, pattern, and evolutionary trade-offs in animal aggregation. , 1999, Science.