animal biodiversity and conservation issue 25.2 (2002)

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ISSN: 1578-665 X An international journal devoted to the study and conservation of animal biodiversity

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  • Form

    erly M

    iscelln

    ia Zoolgica

    2002

    AnimalBiodiversity Conservation25.2

    and

  • Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

    Secretria de Redacci / Secretaria de Redaccin / Managing EditorMontserrat Ferrer

    Consell Assessor / Consejo asesor / Advisory BoardOleguer EscolEullia GarciaAnna OmedesJosep PiquFrancesc Uribe

    Editors / Editores / Editors Pere Abell Inst. de Cincies del Mar CMIMACSIC, Barcelona, SpainJavier AlbaTercedor Univ. de Granada, Granada, SpainAntonio Barbadilla Univ. Autnoma de Barcelona, Bellaterra, SpainXavier Bells Centre d' Investigaci i DesenvolupamentCSIC, Barcelona, SpainJuan Carranza Univ. de Extremadura, Cceres, SpainLus M Carrascal Museo Nacional de Ciencias NaturalesCSIC, Madrid, SpainMichael J. Conroy Univ. of Georgia, Athens, USAAdolfo Cordero Univ. de Vigo, Vigo, SpainMario Daz Univ. de CastillaLa Mancha, Toledo, SpainXavier DomingoRoura Univ. Pompeu Fabra, Barcelona, SpainGary D. Grossman Univ. of Georgia, Athens, USADami Jaume IMEDEACSIC, Univ. de les Illes Balears, SpainJordi Lleonart Inst. de Cincies del Mar CMIMACSIC, Barcelona, SpainJorge M. Lobo Museo Nacional de Ciencias NaturalesCSIC, Madrid, Spain Pablo J. LpezGonzlez Univ de Sevilla, Sevilla, SpainFrancisco Palomares Estacin Biolgica de Doana, Sevilla, SpainFrancesc Piferrer Inst. de Cincies del Mar CMIMACSIC, Barcelona, SpainMontserrat Ramn Inst. de Cincies del Mar CMIMA CSIC, Barcelona, SpainIgnacio Ribera The Natural History Museum, London, United KingdomPedro Rincn Museo Nacional de Ciencias NaturalesCSIC, Madrid, SpainAlfredo Salvador Museo Nacional de Ciencias NaturalesCSIC, Madrid, SpainJos Lus Tellera Univ. Complutense de Madrid, Madrid, SpainFrancesc Uribe Museu de Cincies Naturals de Barcelona, Barcelona, Spain

    Consell Editor / Consejo editor / Editorial BoardJos A. Barrientos Univ. Autnoma de Barcelona, Bellaterra, SpainJean C. Beaucournu Univ. de Rennes, Rennes, FranceDavid M. Bird McGill Univ., Qubec, CanadaMats Bjrklund Uppsala Univ., Uppsala, SwedenJean Bouillon Univ. Libre de Bruxelles, Brussels, BelgiumMiguel Delibes Estacin Biolgica de DoanaCSIC, Sevilla, SpainDario J. Daz Cosn Univ. Complutense de Madrid, Madrid, SpainAlain Dubois Museum national dHistoire naturelleCNRS, Paris, FranceJohn Fa Durrell Wildlife Conservation Trust, Jersey, United KingdomMarco FestaBianchet Univ. de Sherbrooke, Qubec, CanadaRosa Flos Univ. Politcnica de Catalunya, Barcelona, SpainJosep M Gili Inst. de Cincies del Mar CMIMACSIC, Barcelona, SpainEdmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The NetherlandsFernando Hiraldo Estacin Biolgica de DoanaCSIC, Sevilla, SpainPatrick Lavelle Inst. Franais de recherche scient. pour le develop. en cooperation, Bondy, FranceSantiago MasComa Univ. de Valencia, Valencia, SpainJoaqun Mateu Estacin Experimental de Zonas ridasCSIC, Almera, SpainNeil Metcalfe Univ. of Glasgow, Glasgow, United KingdomJacint Nadal Univ. de Barcelona, Barcelona, SpainStewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, SpainTaylor H. Ricketts Stanford Univ., Stanford, USAJoandomnec Ros Univ. de Barcelona, Barcelona, SpainValentn SansComa Univ. de Mlaga, Mlaga, SpainTore Slagsvold Univ. of Oslo, Oslo, Norway

    Secretaria de Redacci / Secretara de Redaccin / Editorial Office

    Museu de Cincies Naturals (Zoologia)Passeig Picasso s/n08003 Barcelona, SpainTel. +34933196912Fax +34933104999Email [email protected]

    Animal Biodiversity and Conservation 25.2, 2002 2002 Museu de Cincies Naturals (Zoologia), Institut de Cultura, Ajuntament de BarcelonaAutoedici: Montserrat FerrerFotomecnica i impressi: Sociedad Cooperativa Librera GeneralISSN: 1578665XDipsit legal: B16.27858

    The journal is freely available online at: http://bcn.cat/ABC

    "Cepaea nemoralis Linneo" Fauna malacolgica terrestre y de agua dulce de Catalua, Dr. F. Haas; Treballs del Museu de Zoologia, 5 (1991). Lmina XLVI.

  • 1Animal Biodiversity and Conservation 25.2 (2002)

    2002 Museu de Cincies NaturalsISSN: 1578665X

    Deharveng, L. & Smolis, A., 2002. Pronura bidoup n. sp. (Collembola, Neanuridae, Neanurinae, Paleonurini)from southern Vietnam. Animal Biodiversity and Conservation, 25.2: 15.

    AbstractAbstractAbstractAbstractAbstractPronura bidoup n. sp. (Collembola, Neanuridae, Neanurinae, Paleonurini) from southern Vietnam. A newspecies of Pronura Delamare Debouteville, 1953, Pronura bidoup n. sp. is described from the Bi Doup massif insouthern Vietnam, where it is largely distributed above 1,350 m. The new species exhibits a combination ofcharacters unusual for the genus: shift of chaeta f towards chaeta e on labium, large central reticulate plate onhead, presence of microchaetae on furcal rest, reduced chaetotaxy of legs and abdominal segment VI. It isrelated to Pronura ornata Deharveng & Bedos, 1993 from high altitude in Thailand.

    Key words: Pronura bidoup n. sp., Collembola, Neanuridae, Vietnam.

    ResumenResumenResumenResumenResumenPronura bidoup sp. n. (Collembola, Neanuridae, Neanurinae, Paleonurini) del sur de Vietnam. Se describe unanueva especie de Pronura Delamare Debouteville, 1953, Pronura bidoup sp. n., del macizo Bi Doup, situado enel sur de Vietnam, donde se distribuye ampliamente por encima de los 1.350 m de altitud. Esta nueva especiepresenta una serie de caracteres poco usuales para el gnero: desplazamiento de la queta f hacia la queta e enel labium, placa central grande reticulada en la cabeza, presencia de microquetas en la base de la furca,quetotaxia reducida en las patas y en el segmento abdominal VI. P. bidoup sp. n. est relacionada con P. ornataDeharveng y Bedos, 1993, que se encuentra a gran altitud en Tailandia.

    Palabras clave: Pronura bidoup sp. n., Collembola, Neanuridae, Vietnam.

    (Received: 7 III 02; Conditional acceptance: 7 V 02; Final acceptance: 6 VI 02)

    1 Louis Deharveng, Museum National dHistoire Naturelle, Laboratoire dEntomologie, ESA 8043 du CNRS, 45rue Buffon, 75005Paris, France.2 Adrian Smolis, Zoological Institute of Wroclaw Univ., Sienkiewicza 21, 50335 Wroclaw, Poland.

    1 Email: [email protected] Email: [email protected]

    Pronura bidoup n. sp.(Collembola, Neanuridae, Neanurinae,Paleonurini) from southern Vietnam

    L. Deharveng1 & A. Smolis2

  • 2 Deharveng & Smolis

    Introduction

    The Bi Doup massif above Dalat in southernVietnam has retained large patches of undisturbedprimary forest, which host a very rich Neanurinaefauna including more than 25 species, all new toscience (Deharveng & Le Cong Kiet, pers. com.). Inthis paper, we describe Pronura bidoup n. sp., amorphologically remarkable species of the genusPronura Delamare Debouteville, 1953, related toPronura ornata Deharveng & Bedos, 1993, knownfrom the top of Doi Inthanon, the highestmountain of Thailand.

    Material and methods

    The terminology and abbreviations used in thetext and the tables are standard conventions fortaxonomic descriptions in the subfamilyNeanurinae (DEHARVENG, 1983, modified).

    Abbreviations used in the text and tables

    Types of chaetae: bms. Buried smicrochaeta; M.Macrochaeta; me. Mesochaeta; mi. Microchaeta;ms. Smicrochaeta; or. Organite of antenna IV; S.Schaeta; x. Labial papilla.

    General morphology: abd. Abdominal segment;ant. Antennal segment; th. Thoracic segment.

    Chaetal groups and tubercles on head: Af.Antennofrontal; CL. Clypeal; De. Dorsoexternal;Di. Dorsointernal; DL. Dorsolateral; L. Lateral ;Oc. Ocular; So. Subocular; Ve. Ventroexternal;Vi. Ventrointernal; VL. Ventrolateral.

    Chaetal groups and tubercles on tergites: De.Dorsoexternal; Di. Dorsointernal; DL. Dorsolateral; L. Lateral.

    Chaetal groups and tubercles of sternites: Ag.Antegenital; An. Anal; Fu. Furcal; Ve. Ventral;VL. Ventrolateral.

    Appendages: Cx. Coxa; Fe. Femur; Scx2. Subcoxa2; Tr. Trochanter; Ti. Tibiotarsus; VT. Ventral tube.

    Types are deposited in the Museum NationaldHistoire Naturelle de Paris.

    Results

    Pronura bidoup n. sp. (tables 1, 2; figs. 16)

    Studied materialHolotype female and one paratype female.Vietnam, Lam Dong province, Bi Doup massif,Nui Gia Rich, 1hr 1/2 from Klong Lanh by foot,1,440 m, litter, Berlese extraction, 18 XII 98, leg.L. Deharveng & A. Bedos (sample VIET689).Types mounted on slides in MarcAndr II.

    Additional specimens (leg. L. Deharveng & A. Bedos)Vietnam, Lam Dong province, Bi Doup massif:1,545 m, litter, Berlese extraction, 28 II 97,

    8 specimens (sample VIET281); ibid: 1,900 m,litter, Berlese extraction, 1 III 97, 2 specimens(samples VIET302, VIET304); ibid: near the schoolof Klong Lanh, 1,410 m, litter, Berlese extraction,18 XII 98, 8 specimens (sample VIET675). Vietnam,Lam Dong province, near Dalat, Cam Ly area,1,380 m, litter, Berlese extraction, 16 XII 98,2 specimens (samples VIET657, VIET665).

    DescriptionLength: 0.55 to 0.75 mm. Colour: white in alcohol.Dorsal tubercles weak or absent; only the tuberclesof head and of abd. V and VI, and the dorsolateral tubercles of abd. IIIV are well developed;they are constituted by stronger secondarygranules, with tertiary granules and slightreticulation on head. In some specimens, secondarygranules are slightly stronger on the axial area ofthe tergites where Di chaetae are more or lessgrouped. Dorsointernal tubercles of abd. V notoverhanging abd. VI. Homochaetotic clothing ofsmooth, slender, tapering and curved meso-chaetae, with frequent asymmetries. Schaetaeon abd. IV thin, 1.5 to 3 times longer thannearby mesochaetae.

    Head (table 1, figs. 1, 2, 4). Schaetae of ant. IVthick and rather short, like in P. ornata (figured inDEHARVENG & BEDOS, 1993); apical vesicle of ant.IVfused to the apex, hardly distinct. Buccal conerather elongate compared to that of P. ornata;labrum rounded at the apex; labium with chaetaeA, C, D, E, F, G, d, e and f, with f closer to e thanto G, and a minute x papilla (fig. 4); chaeta c (orpossibly d) not observed. Maxilla styliform,mandible tridentate. Ocelli either absent, orpossibly 2+2 covered with primary granules andnot clearly distinct from secondary granules. Theclypeal, antennal, frontal and ocular tubercles arefused in a single central plate, with a completeset of chaetae (A, B, C, D, E, F, O, Oca, Ocm, Ocp),and 2 to 4 additional chaetae between A and B,often asymmetrically arranged. Laterally, thetubercles DL, L and So are fused in a unique plate.

    Tergites (table 2, figs. 1, 5). No plurichaetosisnor additional Schaetae. Strong and irregularintegument bumps on abd. IV and sometimes onabd. II between and behind the dorsoexternaland dorsolateral chaetal groups. Dorsointernalchaetae shift towards dorsoexternal ones onabd. V. One lateral chaeta L on abd. V, withouttubercle. Abd. VI not bilobed, with an unevenchaeta and a reduced chaetotaxy.

    Sternites and appendages. Chaeta M absenton tibiotarsi. Vestigial furcal microchaetae of thesternites of abd. IIIIV very distinct, on a smallsmooth plate (fig. 6). Genital plate with 45(female) or 6 (male) circumgenital chaetae, and2 (female) or 4+4 (male) genital chaetae; nomodified chaetae in the male (male specimenfrom VIET281).

    Derivatio nominisThe new species is named after its type locality.

  • Animal Biodiversity and Conservation 25.2 (2002) 3

    Figs. 16. 1, 2, 46. Pronura bidoup n. sp.: 1. Dorsal view; 2. Central plate on head; 4. Labium; 5.Tubercle (Di + De + DL) on abd. V; 6. Furcal rest with its 6 microchaetae. 3. Pronura ornata Deharveng& Bedos, 1993, labium.

    Figs. 16. 1, 2, 46. Pronura bidoup sp. n.: 1. Vista dorsal; 2. Placa central de la cabeza; 4. Labium; 5.Tubrculo (Di + De + DL) del segmento abdominal V; 6. Base de la furca con 6 microquetas. 3. Pronuraornata Deharveng & Bedos, 1993, labium.

    262626262627 27 27 27 27 mmmmm 9 9 9 9 9 mmmmm11111

  • 4 Deharveng & Smolis

    Table 1. Cephalic chaetotaxy of Pronura bidoup n. sp.: G. Group of chaetae; Tu. Tubercle; N. Numberof chaetae; Ty. Type of chaetae; * other chaetae not analysed on ant. IV. .

    Tabla 1. Quetotaxia ceflica de Pronura bidoup sp. n.: G. Grupo de quetas; Tu. Tubrculo; N. Nmerode quetas; Ty. Tipo de queta; * en antena IV no se analizaron otras quetas.

    G Tu N Ty Chaetae

    CL + Af + 2Oc yes 2325 me A, B, C, D, E, F, O, Oca, Ocm, Ocp and 24 additional chaetae

    Di (yes) 1 me Di1

    De yes 3 me De1, Di2, De2

    DL + L + So yes 2 M

    14 me

    Vi 5 me

    Ve 67 me

    Prelabral ? ?

    Labrum basal 2 me

    Labrum distal 2 me

    2 M

    Labium 1 M F

    8 me A, C, D, E, G, d, e, f

    1 x

    Ant. I 7 me

    Ant. II 11 me

    Ant. III 16 me

    2 S S2, S5

    3 ms s1, s3, s4

    Ant. IV* 8 S S1 to S8

    1 bms or

    Table 2. Postcephalic chaetotaxy of Pronura bidoup n. sp.: * 1 mi on the upper valve and ?2 mion the lateral valves.

    Tabla 2. Quetotaxia postceflica de Pronura bidoup sp. n.: * 1 mi en la valva superior y ?2 mi enlas valvas laterales.

    Di De DL L Scx2 Cx Tr Fe Ti

    Th. I 1 2 1 0 3 5 12 18

    Th. II 3 3+S 3+S+ms 3 2 7 5 11 18

    Th. III 3 3+S 3+S 3 2 8 5 10 17

    Abd. I 2 2+S 2 3(4) VT: 4

    Abd. II 2 2+S 2 3(4) Ve: 45 (Ve1 present)

    Abd. III 2 2(3)+S 2 3 Ve: 4 Fu: 3 me, 6 mi

    Abd. IV 2 (1+S, 3) 5 Ve: 8 VL: 4

    Abd. V (S+45) 1 Ag: 3 VL: 1

    Abd. VI (6+6+1) Ve: 11 An: 12 mi*

  • Animal Biodiversity and Conservation 25.2 (2002) 5

    Discussion

    With its clothing of subequal chaetae, its strongocular reduction, its large central plate andsupernumerary chaetae on head and its reducedchaetotaxy on legs and abd. VI, Pronura bidoupn. sp. is close to Pronura ornata Deharveng &Bedos, 1993 from Doi Inthanon in northernThailand. Both are limited to moutain foresthabitats in their respective region. They differin their labial chaetotaxy (chaeta f much closerto G than to e in ornata, closer to e than to G inbidoup), their furcal remnant (microchaetaepresent in bidoup, absent in ornata), and anumber of chaetotaxic details. The labium of P.ornata is quite unusual among Paleonurini, withthe chaeta f shift towards G like in severalother unrelated species of Neanurinae with shortbuccal cones (like Coecoloba sp., figured inDEHARVENG, 1983).

    As the two species share a number ofsingular characters among Paleonurini, we donot however consider this striking differencein labial chaetotaxy to be phylet ical lymeaningful, though it would deserve deeperinvestigation.

    Acknowledgements

    Prof. Le Cong Kiet (University of Ho Chi MinhCity, department of Ecology and Botany) and theForest authorities of Dalat efficiently organisedour expeditions to the Bi Doup massif. UniversitPaul Sabatier and Bourse Germaine Cousin ofthe Socit Entomologique de France financiallysupported part of the field work. We also thankan anonymous reviewer for useful comments onan earlier version of the manuscript.

    References

    DEHARVENG, L., 1983. Morphologie volutive desCollemboles Neanurinae en particulier de laligne nanurienne. Travaux du Laboratoiredcobiologie des Arthropodes daphiques,Toulouse, 4: 163.

    DEHARVENG, L. & BEDOS, A., 1993. New Paleonuraand Pronura species (Collembola, Neanurinae)from Thailand. Zoologica Scripta, 22: 183192.

    DELAMARE DEBOUTTEVILLE, C., 1953. Collemboles duKilimandjaro rcolts par le docteur GeorgeSalt. Ann. Mag. Hist. Nat., 12(6): 817831.

  • Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

    Secretria de Redacci / Secretaria de Redaccin / Managing EditorMontserrat Ferrer

    Consell Assessor / Consejo asesor / Advisory BoardOleguer EscolEullia GarciaAnna OmedesJosep PiquFrancesc Uribe

    Editors / Editores / Editors Antonio Barbadilla Univ. Autnoma de Barcelona, Bellaterra, SpainXavier Bells Centre d' Investigaci i Desenvolupament CSIC, Barcelona, SpainJuan Carranza Univ. de Extremadura, Cceres, SpainLus M Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, SpainAdolfo Cordero Univ. de Vigo, Vigo, SpainMario Daz Univ. de CastillaLa Mancha, Toledo, SpainXavier Domingo Univ. Pompeu Fabra, Barcelona, SpainFrancisco Palomares Estacin Biolgica de Doana, Sevilla, SpainFrancesc Piferrer Inst. de Cincies del Mar CSIC, Barcelona, SpainIgnacio Ribera The Natural History Museum, London, United KingdomAlfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, SpainJos Lus Tellera Univ. Complutense de Madrid, Madrid, SpainFrancesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

    Consell Editor / Consejo editor / Editorial BoardJos A. Barrientos Univ. Autnoma de Barcelona, Bellaterra, SpainJean C. Beaucournu Univ. de Rennes, Rennes, FranceDavid M. Bird McGill Univ., Qubec, CanadaMats Bjrklund Uppsala Univ., Uppsala, SwedenJean Bouillon Univ. Libre de Bruxelles, Brussels, BelgiumMiguel Delibes Estacin Biolgica de Doana CSIC, Sevilla, SpainDario J. Daz Cosn Univ. Complutense de Madrid, Madrid, SpainAlain Dubois Museum national dHistoire naturelle CNRS, Paris, FranceJohn Fa Durrell Wildlife Conservation Trust, Trinity, United KingdomMarco FestaBianchet Univ. de Sherbrooke, Qubec, CanadaRosa Flos Univ. Politcnica de Catalunya, Barcelona, SpainJosep M Gili Inst. de Cincies del Mar CMIMACSIC, Barcelona, SpainEdmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The NetherlandsFernando Hiraldo Estacin Biolgica de Doana CSIC, Sevilla, SpainPatrick Lavelle Inst. Franais de recherche scient. pour le develop. en cooperation, Bondy, FranceSantiago MasComa Univ. de Valencia, Valencia, SpainJoaqun Mateu Estacin Experimental de Zonas ridas CSIC, Almera, SpainNeil Metcalfe Univ. of Glasgow, Glasgow, United KingdomJacint Nadal Univ. de Barcelona, Barcelona, SpainStewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, SpainTaylor H. Ricketts Stanford Univ., Stanford, USAJoandomnec Ros Univ. de Barcelona, Barcelona, SpainValentn SansComa Univ. de Mlaga, Mlaga, SpainTore Slagsvold Univ. of Oslo, Oslo, Norway

    Secretaria de Redacci / Secretara de Redaccin / Editorial Office

    Museu de ZoologiaPasseig Picasso s/n08003 Barcelona, SpainTel. +34933196912Fax +34933104999Email [email protected]

    "La tortue greque" Oeuvres du Comte de Lacpde comprenant L'Histoire Naturelle des Quadrupdes Ovipares, des Serpents, des Poissons et des Ctacs; Nouvelle dition avec planches colories dirige par M. A. G. Desmarest; Brux-elles: Th. Lejeun, diteur des oeuvres de Buffon, 1836. Pl. 7

    Animal Biodiversity and Conservation 24.1, 2001 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de BarcelonaAutoedici: Montserrat FerrerFotomecnica i impressi: Sociedad Cooperativa Librera GeneralISSN: 1578665XDipsit legal: B16.27858

  • 7Animal Biodiversity and Conservation 25.2 (2002)

    2002 Museu de Cincies NaturalsISSN: 1578665X

    Limits to natural variation:implications for systemic management

    C. W. Fowler1 & L. Hobbs2

    Fowler, C. W. & Hobbs, L., 2002. Limits to natural variation: implications for systemic management. AnimalBiodiversity and Conservation, 25.2: 745.

    AbstractAbstractAbstractAbstractAbstractLimits to natural variation: implications for systemic management. Collectively, the tenets and principles ofmanagement emphasize the importance of recognizing and understanding limits. These tenets require thedemonstration, measurement and practical use of information about limits to natural variation. It is importantto identify limits so as not to incur the risks and loss of integrity when limits are exceeded. Thus, by managingwithin natural limits, humans (managers) simultaneously can achieve sustainability and minimize risk, as wellas account for complexity. This is at the heart of systemic management. Systemic management embodies thebasic tenets of management. One tenet requires that management ensure that nothing exceed the limitsobserved in its natural variation. This tenet is based on the principle that variation is constrained by a varietyof limiting factors, many of which involve risks. Another tenet of management requires that such factors beconsidered simultaneously, exhaustively, and in proportion to their relative importance. These factors, incombination, make up the complexity that managers are required to consider in applying the basic principlesof management. This combination of elements is reflected in observed limits to natural variation that accountfor each factor and its relative importance. This paper summarizes conclusions from the literature that hasaddressed the concept of limits to natural variation, especially in regard to management. It describes: 1. Howsuch limits are inherent to complex systems; 2. How limits have been recognized to be important to theprocess of management; 3. How they can be used in management. The inherent limits include both thoseset by the context in which systems occur (extrinsic factors) as well as those set by the components andprocesses within systems (intrinsic factors). This paper shows that information about limits is of utility inguiding human action to fit humans within the normal range of natural variation. This is part of systemicmanagement: finding an integral and sustainable place for humans in systems such as ecosystems and thebiosphere. Another part of sustainability, however, involves action to promote systems capable of sustainablysupporting humans and human activities, not only as individuals, but also as a species. It is important todistinguish what can and what can not be done in this regard.

    Key words: Systemic management, Limits, Variation, Ecosystems, Single species, Resources.

    ResumenResumenResumenResumenResumenLmites a la variacin natural: implicaciones para el manejo o gestin sistmica. En conjunto, los dogmas yprincipios del manejo enfatizan la importancia del reconocimiento y la comprensin de los lmites. Estosprincipios requieren la demostracin, medida y uso prctico de la informacin sobre los lmites de la variacinnatural. Es importante identificar los lmites para no incurrir en riesgos y prdida de integridad cuando dichoslmites se sobrepasan. Con el manejo dentro de unos lmites naturales, el hombre (el responsable del manejo)puede conseguir simultneamente sostenibilidad y minimizacin de riesgos, as como explicar la complejidad.sto est en el ncleo central del manejo sistmico. El manejo sistmico engloba los principios bsicos decualquier tipo de manejo. Uno de los principios requiere que el manejo asegure que nada exceda los lmitesobservados en la variacin natural. Este principio se basa en que la variacin est condicionada por variosfactores limitantes, muchos de los cuales conllevan riesgos. Otro principio del manejo requiere que estosfactores sean considerados simultneamente, exhaustivamente y en proporcin a su importancia relativa.Dichos factores, en combinacin, constituyen la complejidad que los responsables del manejo deben considerar

  • 8 Fowler & Hobbs

    al aplicar los principios bsicos de su funcin controladora. Esta combinacin de elementos se refleja en loslmites observados en la variacin natural referentes a cada factor natural y su importancia relativa. El presenteartculo resume conclusiones extradas de la literatura cientfica respecto el concepto de variacin natural,especialmente en el mbito del manejo describe: 1. En qu medida estos lmites son inherentes a los sistemascomplejos; 2. Cmo se ha reconocido la importancia de estos lmites para el proceso de manejo; y 3. Cmopueden utilizarse para el manejo. Los lmites inherentes incluyen tanto los establecidos por el contexto dondelos sistemas se desarrollan (factores extrnsecos) como los establecidos por los componentes y procesos internosde los sistemas (factores intrnsecos). La informacin sobre los lmites es til como gua de la accin humanapara acomodar los seres humanos al espectro normal de la variacin natural. Esto forma parte del manejosistmico: encontrar un lugar integral y sostenible para el hombre en sistemas tales como los ecosistemas y labiosfera. Otra parte de la sostenibilidad, sin embargo, implica acciones destinadas a promover sistemas capacesde proporcionar apoyo sostenible al hombre y a sus actividades, no slo como individuo sino tambin comoespecie. Es importante distinguir qu puede y que no puede hacerse a este respeto.

    Palabras clave: Manejo o gestin sistmica, Lmites, Variacin, Ecosistemas, Especies individuales, Recursos.

    (Received: 17 IV 02; Conditional acceptance: 30 VII 02; Final acceptance: 13 IX 02)

    1 Charles Fowler, National Marine Mammal Laboratory, Alaska Fisheries Science Center, 7600 Sand PointWay N.E., Bin C15700, Seattle, Washington 981150070, U.S.A.2 Larry Hobbs, P. O. Box 51, Big Pine, CA 93513, U.S.A.

    1 Email: [email protected] Email: [email protected]

  • Animal Biodiversity and Conservation 25.2 (2002) 9

    Introduction

    Considerable time and effort has been devotedto defining ecosystem management (e.g., VANDYNE, 1969; CLARK & SAROKWASH, 1975; AGEE &JOHNSON, 1988a, 1988b; MITCHELL et al., 1990;COSTANZA, 1992; COSTANZA et al., 1992; GRUMBINE,1992, 1994a, 1997; SLOCOMBE, 1993a, 1993b;WOODLEY et al., 1993; MAERZ, 1994; MOOTE et al.,1994; WOOD, 1994; ALPERT, 1995; LACKEY, 1995;MALONE, 1995; PASTOR, 1995; STANLEY, 1995; UNITEDSTATES INTERAGENCY ECOSYSTEM MANAGEMENT TASKFORCE, 1995; CHRISTENSEN et al., 1996; COOPERRIDER,1996; MANGEL et al., 1996; NOSS, 1996; SAMPSON &KNOPF, 1996; SCHRAMM & HUBERT, 1996; NATIONALMARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLESADVISORY PANEL, 1998; COMMITTEE ON ECOSYSTEMMANAGEMENT FOR SUSTAINABLE MARINE FISHERIES,1999; MCCORMICK, 1999 and the referencestherein). This collective effort, in part, was areaction to the trouble that is encountered inpursuing other forms of management, especiallymanagement historically practiced at the single-species level and particularly when managementis aimed at nonhuman species rather thanhumans. These traditional approaches includeresource management with approaches basedon the concept of maximum sustainable yield(MSY, and its failures; LUDWIG et al., 1993;GOODLAND, 1995; CALLICOTT & MUMFORD, 1997;STRUHSAKER, 1998), pest and predator control,and crop management.

    However, management cannot proceed byfocusing on ecosystems to the exclusion ofcomparable consideration of species orindividuals. A form of management is neededthat includes consideration of individuals,species, and the biosphere in other words, allof the various levels of biological organization.These have to be considered in addition toecosystems. If other levels of biological organi-zation are excluded by restricting focus toecosystems, management will get into even deepertrouble than already experienced troublestemming, in part, from a focus that is toonarrow, as experienced by focusing on individualspecies, or on individuals (e.g., individualhumans). Especially problematic is managementthat assumes that humans can control otherspecies or ecosystems and simultaneously avoidthe side effects or unintended consequences ofmanagement action (ROHMAN, 1999). Systemicmanagement (management that embodies theprinciples and tenets of management asdeveloped in the literature on management, torepresent the best thinking available, and asshown in appendix 1; see also: FOWLER, 1999a,1999b; FOWLER & PEREZ, 1999; FOWLER et al.,1999; FOWLER, 2002) avoids these problems byconsidering and accounting for all levels ofbiological organization as part of an applicationof the tenets of management in general. Itextends beyond the management of human use

    of natural resources; it also applies in otherrealms (e.g., CO2 production or energyconsumption: FOWLER & PEREZ, 1999; or socialand psychological issues: JOHNSON, 1992; CONN,1995).

    Management, regardless of its form, is basedon tenets and principles that are seen asimportant. Systemic management is no differentin this regard, and is based, in part, on theprinciple requiring that elements of variousnatural systems be maintained within theirnormal range of natural variation (RAPPORT etal., 1981, 1985; CHRISTENSEN et al., 1996; HOLLING& MEFFE, 1996; MANGEL et al., 1996; FOWLER,1999a, 1999b; FOWLER et al., 1999; MCCORMICK,1999 and references for appendix 2) a themetreated more thoroughly below as a primarypoint in this paper. In developing this point,there is documentation of the recognition ofthis principle, the full history of which deservesmore extensive treatment than is possible here.Part of this history involves the conclusion thatadhering to this principle requires the use ofempirical information about variation and itslimits (FOWLER, 1999a, 1999b; FOWLER & PEREZ,1999; FOWLER et al., 1999).

    The existence of a normal range of naturalvariation implies that there are limits to suchvariability, but does not rule out the possibilitythat natural variation will change over time,space and environmental circumstances (e.g.,weather and climate). Thus, variation is itselfone of the things that varies; but even it haslimits. It is often pointed out that everything hasits limits (PIMENTEL, 1966; HYAMS, 1976; RAPPORT etal., 1981; PIMM, 1982; RAPPORT et al., 1985; SALTHE,1985; ONEILL et al., 1986; SLOBODKIN, 1986;KOESTLER, 1987; CLARK, 1989; GRIME, 1989;ROUGHGARDEN, 1989; ORIANS, 1990; ANDERSON, 1991;MEADOWS et al., 1992; PICKETT et al., 1992; MCNEILL,1993; MOOTE et al., 1994; WILBER, 1995; AHL &ALLEN, 1996; CHRISTENSEN et al., 1996; HOLLING, &MEFFE, 1996; MANGEL et al., 1996; NATIONAL MARINEFISHERIES SERVICE ECOSYSTEM PRINCIPLES ADVISORY PANEL,1998; MULLER et al., 2000; UHL et al., 2000).

    Limits are one of the more recognized elementsof nature, as frequently seen in the study ofecology. Limits define natural patterns. Mostgeneral ecology texts address this concept andmany contain words such as limits, or limitingfactors in their indices (e.g., ALLEE et al., 1949;BROWN, 1995; DIAMOND & CASE, 1986; EMLEN, 1973;KREBS, 1972; ODUM, 1959; PLATT & REID, 1967;RICKLEFS, 1973). Any automated search of theavailable ecological or biological literature byusing the term limits reveals the extent of itsimportance, especially in the titles and key wordsof many papers published in the biologicalsciences. Limiting factors are often treated interms of the constraints posed by availablenutrients, or other resources, but also include theeffects of predation and disease on populationnumbers, biomass, productivity, or species

  • 10 Fowler & Hobbs

    numbers. While the concept is generally welldeveloped in a variety of ecological settings, it ismost commonly used to describe constraints onpopulation size (and the variation of populationnumbers or biomass in space and time).

    Some aspects of limits are straightforward(usually hard limits, see below). A populationcannot use more resources than are available,either in total biomass or numbers of species.Similarly, consuming nothing is not an optionfor any species because zero consumptionguarantees extinction. An ecosystem cannotconstitute more than 100% of the biomass inthe biosphere. Other limits are more complicatedas exemplified by the population dynamics ofany species. The limits set on populations resultin central tendencies (commonly called carryingcapacity, K) such that any species numbersordinarily tend away from zero and cannot beinfinite they find a dynamic balance. These aresystemic limits set by combinations of bothintrinsic and extrinsic factors (INGRAM & MOLNAR,1990), or the soft limits of processes, competingor opposing forces, and related rates. For apopulation, these factors include disease,resource limitations, metabolic needs, densitydependence, social dynamics, life history, bodysize, temperature, habitat, behavior, reproductivestrategy, environmental variation, and predationthe list is virtually endless (PIMENTEL, 1966).

    This paper includes a partial review of theliterature that addresses limits inherent to naturalvariation to help bring the concept of limits toits proper place in management. The followingmaterial presents a much broader perspective,however, than any focus on populations wouldallow. There is a bias, nevertheless, in considera-tion of biological and ecological systems at theexpense of attention to physical systems (e.g.,variation in tidal cycles, climate change, or riverflow). This bias tends to place emphasis on factorsexemplified by consumption of energy (by bioticsystems), consumption of biomass from thebiosphere, production of CO2, and predationrates. It is a primary goal of this paper tostimulate recognition of the concept of limits asa way to guide human action in regard toinfluence on living systems, as well as finding anappropriate place for humans within suchsystems. A major question is faced in manage-ment: Can scientifically meaningful 'limits' or'boundaries be defined that would provideeffective warning of conditions beyond whichthe naturesociety systems incur a significantlyincreased risk of serious degradation? (KATES etal., 2001).

    The sections below begin with a considerationof the terminology used to discuss andcharacterize limits and limitations along withterms used to describe the results of such factors.Following this, there is a section on the factorsthat contribute to limitations those things thatdo the limiting. It contains a sample of what

    collectively comprises the full complexity ofnature or what many call reality. Next is asection containing examples of the kinds of thingsthat are limited. Again complexity or reality isinvolved because virtually everything finite islimited. The fact that there are risks involved inexceeding the normal range of natural variationis emphasized. These risks are among the factorsthat contribute to establishing limits (e.g., thereare risks to each individual human, exemplifiedby the risk of death associated with bodytemperature outside the normal range of naturalvariation). The paper ends with consideration ofthe application of information about limits, therole of such information in management, andthe definition of management based on suchinformation systemic management.

    Terminology

    It is helpful to recognize two categories of limitsintroduced above, each of which will be involvedin the remainder of this paper: soft limits andhard limits. Soft limits arise from a balance offorces or competing rates in natural processes.They are usually invoked long before hard limitsare approached and can be exceeded for variousperiods of time, but not indefinitely. Hard limitsinclude physical limits such as space, or the energycontent of a resource. Thus, true sustainabilityexists only within the combination of limits thatgovern natural systems, each with its own timescale. Temporal scales for soft limits involve thelength of time such limits can be exceeded beforesystemic restorative (homeostatic) forces prevail.

    Appendix 2 presents various quotations fromthe literature where it is seen that a wide varietyof terms are used to deal with the concept oflimits to natural variation. Equivalent terms areused in both the scientific and managementliterature, but in different ways. In scientificpublications, various words are used to representlimits that are identified, observed, describedand measured. Descriptions often include theways in which limitation is brought about by thefactors involved the processes of limitation orthe elements that contribute to limitation. Theterms used in scientific work also describe andidentify the things that are limited. In contrast,the literature on management uses the sameterminology to stress the point that it is importantto do what is possible to maintain systems (suchas ecosystems, and their component species orpopulations) within the normal range of naturalvariation (tenet 3, appendix 1). The literaturealso makes it clear that managers are increasinglyaware that limiting humans becomes bothparamount and the only viable option. It isimportant to limit action so as to avoid risks,including those of doing things that make othersystems fall outside the normal range of theirnatural variation (appendix 1, MCCORMICK, 1999).

  • Animal Biodiversity and Conservation 25.2 (2002) 11

    Constrain

    Variations on this term are often used tocharacterize nature and natural processes(appendix 2; FARNWORTH & GOLLEY, 1974; ALLEN &STARR, 1982; PIMM, 1982, 1984; SALTHE, 1985; FISHER,1986; ONEILL et al., 1986; STEARNS, 1986; BROWN &MAURER, 1987; GLAZIER, 1987; KOESTLER, 1987; AGEE& JOHNSON, 1988a; GRIME, 1989; GRUBB, 1989;TILMAN, 1989; BURNS et al., 1991; PONTING, 1991;HANNON, 1992; NARINS, 1992; BROWN, 1995; AHL &ALLEN, 1996; HOLLING & MEFFE, 1996; MANGEL etal., 1996; MULLER et al., 2000). As will be seenbelow, systems place limits on their componentsand the term constrain is used along with othersto convey this concept (e.g., BURNS et al., 1991).Constraining effects are involved in speciesinteracting with each other (e.g., KNOLL, 1989).The term constrain is also used in the literatureon management but it is applied in two ways.First, it is used in terms of action (constraininghuman options, and as a matter of exhibitingconstraint). Second, it is used interpretively. Thatis, empirical information observed in scientificstudies is seen as guidance for action what toachieve in carrying out constraining action. Theguidance to be used in management is providedby information about natural limits (AGEE &JOHNSON, 1988a; PICKETT et al., 1992; PONTING,1991; CHRISTENSEN et al., 1996; FOWLER et al.,1999).

    Limit, limitations, limiting

    These words, and other derivatives of the wordlimit are used often, again both with respect tocharacterizing nature (DARWIN, 1953; PIMENTEL,1966; BATESON, 1972; HYMANS, 1976; LEVINTON,1979; STANLEY et al., 1983; YODZIS, 1984; ONEILLet al., 1986; AGEE & JOHNSON, 1988a; BUSS, 1988;CLARK, 1989; ROUGHGARDEN, 1989; ORIANS, 1990;WOODWELL, 1990; ANDERSON, 1991; PONTING, 1991;PICKETT et al., 1992; MCNEILL, 1993; SWIMME &BERRY, 1994; WOOD, 1994; ROSENZWEIG, 1995; AHL& ALLEN, 1996; CHRISTENSEN et al., 1996; NATIONALMARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLESADVISORY PANEL, 1998) and as important tomanagement (HYMANS, 1976; AGEE & JOHNSON,1988a; ANDERSON, 1991; PONTING, 1991; PICKETT etal., 1992; MCNEILL, 1993; MOOTE et al., 1994;WOOD, 1994; HARDIN, 1995). The concept ofmanagement as a process of limiting humaninfluence is interwoven with the observationand characterization of natural limits.

    Threshold, boundary, border

    The concept of limits is also embodied in wordsthat refer to transition points (see the use ofthese words or their derivatives in referencessuch as BROWN, 1995; BROWN & MAURER, 1989;CLARK, 1989; ELDREDGE, 1991; HASSELL & MAY, 1989;HENGEVELD, 1990; FUENTES, 1993; MANGEL et al.,

    1996; NATIONAL MARINE FISHERIES SERVICE ECOSYSTEMPRINCIPLES ADVISORY PANEL, 1998; SALTHE, 1985). Inpredator/prey interactions, for example, thereare various component processes that result incyclic or chaotic population dynamics when theyexceed certain levels, often referred to asthresholds or boundaries, also reflected in certainforms of singlespecies population dynamics (e.g.,HASSELL et al., 1976). However, bounds and bordersalso refer to the combination of upper and lowerlimits that confine sets of viable options (BOTKIN& SOBEL, 1975; CHRISTENSEN et al., 1996). As withother terms, these are also used both in definingand guiding the process of management (e.g.,see SCHAEFFER & COX, 1992; FUENTES, 1993) as wellas in scientific characterization of nature.

    Control

    This word is also used in reference to the conceptof limits, especially in regard to the constrainingeffects of a systems influence on its components(e.g., KOESTLER, 1987; ONEILL et al., 1986; SALTHE,1985; WILBER, 1995). The collective effects of allparts of a system on any one part are greaterthan the effects of the one on any other (singlepart). Following this observation, it is recognizedthat management cannot ignore the fact thathuman influence on one component of anycomplex system results in indirect effects onother parts of the system as well as those systemsin within which it occurs (secondary effects:PIMM & GILPIN, 1989; second order effects, rippleeffects: DIAMOND, 1989; nonlinear effects,domino effects: STANLEY, 1984; down streameffects, delayed effects, side effects: PONTING,1991 all parts of the unintended consequencesof human influence: ROHMAN, 1999) and controlis seen as a concept restricted primarily to humanendeavor (HOLLING & MEFFE, 1996; MANGEL et al.,1996). Humans have no control over othersystems in the sense that no one can change thefact that there will always be secondary (orhigher order) effects of human influence, evenwhen control is attempted. This includes thefeedback of such effects on humans. There arealways unintended consequences (ROHMAN, 1999)to management action and one of the limitsexperienced in management is the inability tochange this fact.

    Other terms used in regard to limits andlimiting processes include regulated (LEVIN, 1989),governed, restricted, restrained, confined,proscribed, suppressed, curtailed, channeled,circumscribed, curbed, contained, barriers (CLARK,1989), and resistance.

    Still more terms are involved in characterizingthe results of limitations seen in the empiricallyobserved limits to variation. Such characteristicsare the qualities of the limits seen in variation(e.g., range spanned), and the kinds of variationobserved (e.g., bimodal or unimodal) within thenormal ranges of variation between upper and

  • 12 Fowler & Hobbs

    lower limits. Natural variation is constrained byboth upper and lower limits. Limits, constraintsand risks do not always increase or decreasemonotonically. The combined effects of thenumerous limitations, as they act in concert, areeven more complicated. An example that is easyto relate to as individual human beings is therisk of mortality from various factors risks thatincrease for body weight, blood pressure, andbody temperature both above and below themidpoints of the ranges that they span (e.g., seeCALLE et al., 1999, and references therein,regarding weight). Therefore, upper and lowerlimits preclude many options; they function toallow as the only viable alternatives those seenbetween upper and lower limits. The remainingoptions are usually realized with their greatestfrequency at some midpoint between the limits.Thus, there is always an emergence of centraltendencies between upper and lower limits.Limits often operate as opposing forces (oftensoft limits), and the collective balance found insuch opposition contribute to the formation ofpatterns in nature (e.g., see the stochastic analogof equilibrium; BOTKIN & SOBEL, 1975; CHRISTENSENet al., 1996). There is terminology associatedwith these patterns, or central tendencies, justas there is for the consideration of any singlecomponent among the factors that contribute tolimiting natural variation.

    Mean, mode and median

    Statistical names for the measure of centraltendencies include terms such as these (SNEDECOR,1956) to refer to the magnitude of the centraltendency (i.e., its position) within the infiniterange of options among real numbers.

    Kurtosis and skewness

    These terms refer to the position and concentrationof central tendencies with respect to the upperand lower bounds of variation (SNEDECOR, 1956).Kurtosis refers to the distance between the centraltendency and its limits, the concentration ofobserved measures near the central tendency, orthe flatness and spread of the distribution.Skewness relates more to the degree to whichthere is a lack of symmetry in the variation. Thus,both terms are used in regard to the shape of thefrequency distribution (or probability distribution)of empirically observed variation. Variousmathematical models (e.g., log normal, binomial,Poisson, and others, SNEDECOR, 1956) are availableto represent the probability distribution of variationin its different forms. Transformations are oftenused to convert measures showing nonsymmetricdistributions to more symmetric or normaldistributions (especially log transformations, LIMPERTet al., 2001).

    Terminology is not confined to the concept oflimits, measures of limits, or the characterization

    of variation within limits as treated above.Various terms are also used in reference to theprocesses that contribute to the production ororigin of central tendencies, especially theirpositions. Naturally, these include the limitingprocesses that affect constraint above and belowthe central tendencies. However,, such processesalso include other factors, such as processesinvolving replication or positive feedback thatcontribute to the position of central tendenciesthrough the accumulation of more numerousexamples in the regions of central tendencies.

    Homeostasis, balance and feedback

    These terms are examples of words regardingthe processes that contribute to the origins ofcentral tendencies (as opposed to simpleconstraint). Specific examples of the elementsinvolved in these processes will be consideredbelow. These processes operate in conjunctionwith all other processes in nature as none canoperate in isolation from the others. The resultsof the synergistic combination of all the processesare the patterns observed to characterize nature(ALLEN & STARR, 1982) often seen as emergentpatterns (KAUFFMAN, 1993; ELHANI & EMMECHE,2000) that include the stochastic analog ofequilibrium (BOTKIN & SOBEL, 1975; CHRISTENSEN etal., 1996). These processes are part of what thevarious species (including humans, tenet 9,appendix 1) are exposed to by being part ofsystems such as ecosystems.

    Integrity, balance and normal (or natural)

    These are terms related to such patterns as thosethat make up, or characterize, natural systems(e.g., GRUMBINE, 1994a) often found in the titlesof papers describing nature (e.g., WILLIAMS, 1964).Many of these patterns are correlative, meaningthat the magnitude of the mean of a variable isrelated to that of another variable (measure) asexemplified by the relationship between thecentral tendency of population density and bodysize for animals (fig. 1, see also DAMUTH, 1987;PETERS, 1983). Others relate to the physicalenvironment as found in relationships betweengeographic range size and latitude (e.g., STEVENS,1992) or predation rates and temperature. Theword integrity is sometimes used with regard tomanagement objectives in the sense of achievingnormal states of nature (e.g., KARR, 1990). Balanceis often seen as a property of nature in view ofthe limits to variation (e.g., PIPER, 1993) andsomething that occurs in spite of variation (i.e.,equilibria are rarely static properties of nature,especially biological systems; BOTKIN & SOBEL, 1975;CHRISTENSEN et al., 1996).

    There is yet another set of terms used tocharacterize statistical outliers, extremes, orthings beyond the normal range of naturalvariation (e.g., beyond the limits, MEADOWS et

  • Animal Biodiversity and Conservation 25.2 (2002) 13

    al., 1992), especially as cases subject to the risksof limiting factors and include words such asabnormal, pathological, deviant, aberrant,atypical, and anomalous. The word unnatural isalso used but must be treated with care.Everything happens naturally and extremesbeyond the normal ranges of natural variationare subject to the natural limits and risks thatmake such extremes rare. Thus, it is not so muchunnatural, as it is abnormal, to observe acharacteristic or condition (such as a fever) as anextreme. Extreme fluctuation is abnormal(CHRISTENSEN et al., 1996) as is often observed forpopulations. Thus the term pathological, orcarcinogenic is used in reference to humanoverpopulation (CALHOUN, 1962; BATESON, 1972;HERN, 1993). At the ecosystem level pathology isalso used to describe problems when atypicalconditions arise (e.g., RAPPORT, 1989a). These arewords that help clarify the distinction betweenthe natural occurrence of extremes and thingsthat fall in the normal range of natural variation.

    Factors contributing to limits: complexity I

    Limiting factors combine in nature to make up aninterconnected set of forces, risks, and constraints.A major part of scientific endeavor is dedicatedto documenting these factors and the lists thatare available now, while long, only scratch the

    surface of the complexity of reality even intheir combination. The entire complexity withinand among natural systems contributes to boththe collective constraints on variation and to theformation of the central tendencies within suchvariation (e.g., see PIMENTEL, 1966 regarding limitsto population size) as introduced above. Researchon the limits to variation in biological systems hasresulted in the recognition of a great manycontributing factors and an exhaustive list isbeyond the scope of this paper. However, thereare examples worth mention, some of which arefound in appendix 2.

    A great deal of literature has accumulatedfrom studies of the factors that limit populationsize. There is a long list, and various categories ofsuch factors are considered to be of importance.Among such categories are parasites, predators,disease, behavior (COHEN et al., 1980), energy,resources (food, prey), space, competition, andnutrition (including needs for individual elementsand their compounds such as amino acids) allsubjects of a long history of research on populationecology and represented by a sample of referencesin appendix 2 (e.g., PIMENTEL, 1966; FARNWORTH &GOLLEY, 1974; ONEILL et al., 1986; TILMAN, 1989;MCNEILL, 1993). Other factors include limits on theoptions for life history strategy especially as relatedto body size (DAMUTH, 1987), or the options forpopulation growth and kinds of mortality asrelated to life history strategy (FOWLER, 1988).

    Fig. 1. Population density of 368 terrestrial mammalian herbivore species in relation to adultbody mass (DAMUTH, 1987; FOWLER & PEREZ, 1999) as an example of variation in one measure ofa species in relationship to variation in another.

    Fig. 1. Densidad de poblacin de 368 especies de mamferos herbvoros terrestres en relacin conla masa corporal de los adultos (DAMUTH, 1987; FOWLER & PEREZ, 1999) como ejemplo de variacinde una medida en una especie respecto a la variacin en otra especie.

    33333 22222 11111 00000 11111 22222 33333 44444logloglogloglog1010101010(body mass, kg)(body mass, kg)(body mass, kg)(body mass, kg)(body mass, kg)

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  • 14 Fowler & Hobbs

    The limitation of populations by micro-organisms (diseases or pathogens) or other pestshas been of special focus in many studies and arefactors recognized by PIMENTEL (1966), FARNWORTH& GOLLEY (1974), STANLEY et al. (1983), and TILMAN(1989). A review of such limitations has beenconducted by MCCALLUM & DOBSON (1995).However, it is clear that microscopic or smallbodied consumers are not the only category ofspecies known to contribute to the limitationson the population size of their hosts. Consumerspecies that are of larger body size than theirconsumed prey/resources are also involved (e.g.,predators and herbivores; STANLEY et al., 1983;ONEILL et al., 1986; MCNEILL, 1993). Whethermicroscopic or not, the degree to which onespecies acts to limit the population of anothervaries from case to case. Removing predatorsexperimentally to rid their resources of suchinfluence often results in population increases,but not always. Limiting influence is thus only atendency and rarely predictable owing to thecomplicated nature of the interactions and factorsthat influence them (PIMM, 1991). In the finalanalysis, mortality caused by consumers or diseasecount among the many factors that contributeto limiting population size but are not the onlyfactors involved.

    Sunlight provides the energy that is passedthrough the food webs of communities andecosystems. This energy is involved in metabolism,growth, reproduction and survival. It is notlimitless in its flow through biological systems,however, and is among the factors that havebeen studied for a variety of such systems fromcells to the biosphere. As such, energeticconstraints are not confined to setting limits onpopulation size and the various limits involvingenergy are represented by a voluminousliterature. Energy has been noted as a limitingfactor in a variety of biological systems by BROWN(1981), PIMM (1982, 1984), YODZIS (1984), BROWN& MAURER (1987), GLAZIER (1987), GASTON (1988),TILMAN (1989), and HANNON (1992). Energy isclearly not the only limiting factor for biologicalsystems. The more general issue of resources(including nutrients of various kinds) asconstraining factors is often noted (STANLEY etal., 1983; ONEILL et al., 1986; MCNEILL, 1993),occasionally as expressed through competition(PIMENTEL, 1966; STANLEY et al., 1983).

    Another important resource is space (or habitatsize). Thus, space is also frequently identified asa limiting factor, including its limitations onspecies numbers in addition to its constraints onpopulation size (e.g., STANLEY et al., 1983; ONEILLet al., 1986; ROSENZWEIG, 1995; BROWN, 1995).

    Extinction is also a limiting factor (BROWN &MAURER, 1987), perhaps an ultimate limiting factor(at times a soft limit with a long time scale), andone that has its effects on species numbers,diversity, communities (ARNOLD & FRISTRUP, 1982;FOWLER & MACMAHON, 1982; GOULD, 1982;

    ELDREDGE, 1985; KITCHELL, 1985; LEVINTON, 1988;BROWN, 1995; ROSENZWEIG, 1995), and body size(i.e., as a contributing factor in limiting themaximum size observed among species, e.g., seeVAN VALEN, 1973; BARANOSKY, 1989; FOWLER &MACMAHON, 1982; BROWN, 1995). Thus, extinctionat the specieslevel, like death at the individuallevel, is one of the risks associated with theextremes characterized as pathological orabnormal. Extinction is a limiting factor thatalso exemplifies a process rather than a physicalentity in its limiting action (soft limit in involvinglong time scales).

    Other limitations involve morphological factors(PIMM, 1982, 1984; FISHER, 1986; BROWN, 1995),functional, historical, and evolutionary elements(PICKETT et al., 1992), physiology, and behavior(BROWN, 1995), various population dynamical forces(as well as other dynamics; PIMENTEL, 1966;LEVINTON, 1979; PIMM, 1982, 1984; ROSENZWEIG,1995), environmental predictability (LEVINTON,1979), environmental heterogeneity (PIMENTEL,1966), evolutionary forces (including geneticfeedback mechanisms, PIMENTEL, 1966; FOWLER &MACMAHON, 1982; PIMM, 1984), and the availabilityof genetic (raw) material (GRUBB, 1989). Nutrition,space, toxic materials, competition, predation,cannibalism, and stress are all limiting factors(ROSENZWEIG, 1974). There is little, if anything,that can be ignored in the complexity of factorsthat limit variability (PIMENTEL, 1966).

    It must be recognized that there are two moreclosely interrelated categories of limiting factors(each involving both hard and soft limits)depending on whether they are extrinsic orintrinsic to the system showing variation (INGRAM& MOLNAR, 1990). Variation limited by extrinsicfactors in biological systems includes the effectsof disease, predation, competition, habitat size,and resource availability on population size.Intrinsic factors limiting population size include,body size, behavior, and the birth and death ratesinvolved in life history strategies. At the sametime such factors are observed to contribute tolimitations, they also have their influence on theposition of central tendencies. Intrinsic andextrinsic factors are involved in the limitation ofany system and its interactions with other systems.

    As amplified in the next section, there are avariety of levels of biological organization towhich limiting factors apply. These span therange from subcellular structures, to cells,organs, individual organisms, populations,species, communities and ecosystems, throughto biomes and the biosphere. It is easy to findexamples of limiting factors for each level ofbiological organization. At the individual level,body size is limited by extrinsic factors such asfood availability, and intrinsic factors such asmetabolic dynamics. This list goes on to includemortality at the individual level, and extinctionat the species level. At the community orecosystem level, species numbers are limited

  • Animal Biodiversity and Conservation 25.2 (2002) 15

    extrinsically through factors exemplified by energyand space, and intrinsically by evolutionary factorsand population dynamics. Collectively, all speciesin an ecosystem interact with each other suchthat each one is subject to the constraintsemergent from the combined effects of the others.This happens in all systems such that the extrinsicfactors that impose limits include those throughwhich a system poses limits to its parts or itscomponents (e.g., AHL & ALLEN, 1996; MULLER etal., 2000). These include the processes of naturalselection involving death and extinction.

    Both intrinsic and extrinsic factors operatesimultaneously and collectively in natural systems(INGRAM & MOLNAR, 1990) sometimes reinforcing,sometimes nullifying each other. The degree towhich such things happen varies from case tocase. Furthermore, synergistic effects andinteractions among such factors are common. Thecombined action of such factors result in observedpatterns (e.g., as observed in the results of variousforms of natural selection; ARNOLD & FRISTRUP,1982; FOWLER & MACMAHON, 1982; GOULD, 1982;LEVINTON, 1988). Thus, patterns are the results ofsystemic effects, or the effects of the entire suiteof limiting factors and all of their interactions.Some of these patterns in nature are partiallyexplained by the balances that result from limitingfactors that function to reinforce or oppose oneanother. Balances resulting from the latter areespecially important in observed patterns.Extinction acting to limit the options for naturalselection at the individual level provides a goodexample (ALEXANDER & BORGIA, 1978; FOWLER &MACMAHON, 1982; GOULD, 1982; LEVINTON, 1988).Other patterns result from parallel, or reinforcing,effects. Examples of factors that may work inconcert are seen in the interplay of body size,population size and geographic range (BROWN &MAURER, 1987; GASTON & BLACKBURN, 2000) onextinction rates. Species of large body size andspecies with small geographical ranges appear tohave higher extinction rates. This may contributeto there being fewer species that are large bodiedwith small geographic ranges compared to specieswith small bodies and large ranges.

    The things with constrained variation:complexity II

    Limitations are imposed on all components andprocesses at each level of biological organization.Whether it be a cell, physiological process,population, predation rate, total populationbiomass, speciation, or number of species, it issomething with variation that is subject to limits.This section turns from the things that exert limitinginfluences reviewed in the previous section toexamples of the things that are subject tolimitations. These include such things as body size,blood pressure, and heart rates for individualanimals. The components of ecosystems and

    ecosystems themselves are also subject to limitations(NATIONAL MARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLESADVISORY PANEL, 1998; HAGEN, 1992).

    Population size and population variation arelimited. There is a voluminous literature treatinglimits to population size (e.g., HOLLING, 1966;PIMENTEL, 1966; FARNWORTH & GOLLEY, 1974; ONEILLet al., 1986; GLAZIER, 1987; SINCLAIR, 1989; TILMAN,1989) that cannot be ignored. Many things thatlimit population size per se are also factors thatlimit population variation which is limited withinspecies as well as among species (SPENCER & COLLIE,1997; FOWLER & PEREZ, 1999). Variation in generalis limited and population variation is an example(BUSS, 1988; HOLLING, 1966; ONEILL et al., 1986).The results of work on populations serve as anexample of insight that would be expected forother aspects of biological systems had theybeen the subject of equivalent study.

    Other factors are far from ignored, however. Inaddition to population size and variation, the limitsin variation have been shown for a variety ofbiological processes and dynamics. The evolutionaryprocess is not free of limitations (e.g., GRUBB, 1989).For example, the extent of evolutionary change islimited (FISHER, 1986) because evolution ischanneled by various constraints (GRIME, 1989).The general concept is exemplified by the lack ofevolutionary options as limited by cell structure.There are no single celled organisms that weigh ametric ton. Other processes are also limited. Thebehavior of organisms and its evolution is limited(NARINS, 1992). The variety of dynamics of (andwithin) communities and ecosystems are limited(LEVIN, 1989; PIMM, 1982). These include the flow ofenergy among species (owing to the limitationsestablished by the inefficiency of metabolic,photosynthetic, and digestive processes). As willbe seen, processes such as predation, CO2production, reproduction and mortality all fit withinlimits.

    The size of cells and the qualities of individualorganisms are limited just as the qualities ofpopulations and ecosystems are (again by bothintrinsic and extrinsic factors, INGRAM & MOLNAR,1990; HAGEN, 1992; TILMAN, 1989). The charac-teristics and qualities of species are limited by,among other things, a variety of evolutionaryprocesses as well as intrinsic factors. Amongspecies groups, attributes are limited by selectiveextinction which often involves intrinsic andextrinsic factors operating in concert (ARNOLD &FRISTRUP, 1982; FOWLER & MACMAHON, 1982; GOULD,1982; STANLEY et al., 1983; LEVINTON, 1988). Thereare limits to diversity (HUTCHINSON, 1972; INGRAM& MOLNAR, 1990).

    Other factors that are subject to limits includerange size (PAGEL et al., 1991; STANLEY, 1989;GASTON & BLACKBURN, 2000), the total number ofspecies (VALENTINE, 1990) and length of foodchains (PIMM & LAWTON, 1977; LEVINTON, 1979;PIMM, 1984; YODZIS, 1984). Variation within andamong ecosystems and that of ecological

  • 16 Fowler & Hobbs

    communities are constrained by the influence offactors such as selective extinction (ALEXANDER &BORGIA, 1978; FOWLER & MACMAHON, 1982; ARNOLD& FRISTRUP, 1982; GOULD, 1982; ELDREDGE, 1985;KITCHELL, 1985; LEVINTON, 1988; HERRERA, 1992;GASTON & BLACKBURN, 2000), including limitationson the numbers of species (e.g., the size of themembership of a community as the count ofspecies, ROUGHGARDEN, 1989; GLAZIER, 1987) orspecies richness (LEVINTON, 1979). The numbers ofspecies consumed by a consumer and the numberof consumers that consume a particular preyspecies are constrained (MARTINEZ, 1994). Thequalities of species involved in communities andecosystems are limited as exemplified by thesmall number of species with large body sizecompared to smallbodied species (FOWLER &MACMAHON, 1982; BROWN & MAURER, 1987). Withincommunities and ecosystems the number oftrophic levels are limited (ROSENZWEIG, 1995).Constraints influence most of the patterns anddynamics of (and within) communities andecosystems (LEVIN, 1989; PIMM, 1982).

    The components of systems are limited, amongother things, by the systems of which they are apart. There is a substantial body of literature thatpresents a helpful interpretation of the collectiveeffects of limiting factors that is, the limitationsresulting from the suite of all factors actingtogether, regardless of what is being limited. Insuch work, it is pointed out that the collectiveeffects of complex systems control, constrain orotherwise limit their components (e.g., DYLE, 1988;KOESTLER, 1987; ONEILL et al., 1986; SALTHE, 1985;WILBER, 1995; MULLER et al., 2000). An examplewould be the limiting influence of an ecosystemon its component species and their populations(ONEILL et al., 1986).

    Such work adds to the importance of theobservation that everything is subject to limits.Everything (everything finite) is part of a moreinclusive system which includes all of the factorsthat contribute to setting limits. Thus, withinbiological systems, each thing chosen for scientificstudy will be limited by the more inclusive orcollective level of biological organization of whichit is a part, along with the nonbiological elementsand processes of its environment (sometimesreferred to as context, appendix 1). This is amatter of scale as noted by AHL & ALLEN (1996)who point out that smallscale entities are limitedby the larger scale entities. Much of the literaturemakes the point more generally: all componentsof more inclusive systems are limited by thecollective influence of the factors to which theyare exposed (e.g., BATESON, 1972; ALLEN & STARR,1982; MAYR, 1982; SALTHE, 1985; ONEILL et al.,1986; KOESTLER, 1987; BUSS, 1988; ORIANS, 1990;BURNS et al., 1991; MCNEILL, 1993; AHL & ALLEN,1996; MULLER et al., 2000). And everything finite isa component of some larger system (WILBER, 1995).It must be concluded that everything is subject tolimits in its natural variation.

    Personal experience emphasizes this fact.Perhaps this is recognized most clearly in observingthat humans are limited in what can be known(FOWLER et al., 1999) or what can be conceptualized(MCINTYRE, 1997). Thus, not only are there limitsto what can be done and what humans can be,but humans are limited in what can be understood.Knowledge itself is limited. In part, the experienceof these limits, along with other limitations, isrelated to the fact that finite things are, by theirvery nature, limited. The models used to representthings can not be all inclusive and the results ofexercises based on models are thereby subject toerror; being limited, models are real but notreality, just as maps are not the territory (BATESON,1972, 1979; models are never the reality theyrepresent). Thus, science is limited. This isexperienced in the inability to recombineinformation from the things that are studied(what might be called the HumptyDumpty effect,or syndrome, NIXON & KREMER, 1977; DUNSTAN &JOPE, 1993; REGAL, 1996; HORGAN, 1999). Even moreof the limits of science are experienced in theinability to adequately or accurately assignimportance to the influence (limiting or otherwise)of each factor made the focus of research (ALLEN& STARR, 1982; BARTHOLOMEW, 1982; ROSENBERG,1985; SALTHE, 1985; GROSS, 1989; PETERS, 1991;PICKETT et al., 1994).

    There is a continued experience of limitationsin progression from science (e.g., PETERS, 1991;STANLEY, 1995) to management. As alreadymentioned, the options for management arelimited in that humans cannot control the factthat there will always be unintended consequencesto management action. There is no control overother systems to avoid such effects. The tenets ofmanagement limit what can be done; they arebased on principles that exert a form of naturalselection among the options. Humans are limited,as in everything else, in management. It is time tomanage with limits in mind.

    Utility / practical application

    Patterns arise, in part, from the limits to variationresulting from the vast array of inter-relationshipsamong the various elements of nature operatingsimultaneously. Variation itself, both within, andas a part of pattern, is also a product of thiscomplexity. Everything is subject to the influenceof the elements in its environment (context,BATESON, 1972, and extrinsic factors) along withthe influence of its components (WILBER, 1995;intrinsic factors). Are these observations of nomore than philosophical interest? Many can beeasily documented or experienced personally,but of what use are they?

    One tenet of management requires that things(e.g., biological systems and processes) bemaintained within the normal range of naturalvariation (tenet 3, appendix 1). There is an

  • Animal Biodiversity and Conservation 25.2 (2002) 17

    especially important element of responsibility forimplementing this element of management withrespect to biological systems. Such requirementshave long been recognized in human andveterinary medicine. This is now being extendedto ecosystems and all of their components,including humans (e.g., CHRISTENSEN et al., 1996;MANGEL et al., 1996; MCCORMICK, 1999, appendix 1and 2). Various panels and groups convened toaddress the management process (especially atthe ecosystem level) have reached the conclusionthat this is an essential tenet of management(e.g., NATIONAL MARINE FISHERIES SERVICE ECOSYSTEMPRINCIPLES ADVISORY PANEL, 1998, appendix 2). MOOTEet al. (1994) were clear that ecosystems and naturalpatterns are the result of limits and that humanshave the responsibility to fall within such limits.Managers are responsible for doing what can bedone to ensure that ecosystems fall within thenormal range of natural variation. However, thisconclusion is not restricted to individuals, species,ecosystems or communities. It applies to nature(e.g., combinations of biological systems) ingeneral (e.g., DARWIN, 1953; PICKETT et al., 1992;SALZMAN, 1994; WOOD, 1994; CHRISTENSEN et al.,1996; NATIONAL MARINE FISHERIES SERVICE ECOSYSTEMPRINCIPLES ADVISORY PANEL, 1998). Managementshould be carried out by doing everything possibleto ensure that biological systems fall within theirnormal range of natural variation. Doing so is atthe core of systemic management.

    Part of the concept of normal involves what isnatural. Much of the literature on managementemphasizes the importance of doing things tomaintain or recover natural states regardless ofwhether it is for individuals, species, communitiesor ecosystems. Recent literature regardingecosystems illustrates the progression in thedevelopment of this concept from its acceptanceat the individual level to its application at higherlevels of biological organization (HOLLING & MEFFE,1996; MANGEL et al., 1996; RAPPORT et al., 1981,1985; DAVIS & SIMON, 1994; CHRISTENSEN et al., 1996;FOWLER, 1999a, 1999b; FOWLER et al., 1999). Theword intact is used to refer to systems that arehealthy or undamaged (ANDERSON, 1991). Suchconcepts are meaningless without frames ofreference. Thus, natural patterns are often seenas those that fall within the normal limits ofvariation, not only for physical structure but also fornatural processes. There is need for care here. It isimportant to be mindful of the fact that it is naturalfor there to be occasional outliers as examplesbeyond the normal range of natural variation andwhen such occasions arise, they are subject to thenatural effects of limits (i.e., the natural phenomenathat set limits, pose risks, and prevent the occurrenceof more such extremes risks exemplified by deathand extinction).

    It is also important to account for humaninfluence. There are few if any systems left on theplanet that have not been subjected to abnormalhuman influence and the problem of providing

    reference points is growing (DAYTON, 1998).However, all species influence their ecosystemsand the other species in such systems. The extentof human influence would not be a particularlylarge problem if anthropogenic effects were notthemselves abnormal as will be seen in the sectionsahead. As a result of the extensive humaninfluence it is important to define normal andnatural so as to focus more on situationswherein human influence itself is not abnormal;that is, within the range of natural variation ofinfluences that other species exhibit.

    Attempts to apply the concepts of normaland natural include efforts to return ecosystemsto normal states. However, restoration (e.g.,ecosystem restoration, JORDAN et al., 1987) cannotbe a recovery of the past a clear hard limit isthe irreversibility of time. It is possible to learnfrom history, and seek guiding information frompatterns historically observed, but it is impossibleto reconstruct what existed in the past. Changeis a permanent part of the processes that cannotbe avoided, especially change resulting fromaction taken in management.

    When considering management, it is impossibleto escape the concept of what should be andhence, the matter of ethics. The material presentedhere is based on the assumption that the tenetsthat have been accepted in the literature are, infact, important. Tenet 3 (appendix 1) emphasizesthe importance of acting so as to facilitate anybiological systems falling within its normal rangeof natural variation (whether such a system be acell, organ, individual, population, species,ecosystem or the biosphere). It is worth pointingout, however, that there are religious elements tothe ethic behind this tenet that are of longstanding importance (e.g., CLARK, 1989; PONTING,1991). An indepth treatment of ethical issues, ortheir history, is beyond the scope of this paper.

    Another tenet of management is that of havingmeasurable goals and objectives; there need to benorms, standards, reference points, guidelines andcriteria to go by (tenet 7, appendix 1). These areprovided through systemic management: thecentral tendencies and statistical confidence limitsobserved in natural variation provide such guidance.They represent options that are optimal inminimizing risk not just any particular set, butall risks working in concert. These risks andconstraints are the entire suite of factorsexperienced by systems such as cells, species, orindividuals in the real world. Thus, the empiricallyobserved central tendencies fall between the upperand lower limits observed for variation subject tothe all limiting factors of the real world actingsynergistically. Therefore, understanding limits, andtaking advantage of the results of their action,provides a great deal to go on in this regard andprovides hope of implementing sound management(DARWIN, 1953).

    This is the concept behind the medicalperception of health when action is taken to

  • 18 Fowler & Hobbs

    restore body temperature, blood pressure, or bodyweight that is abnormal. Thus, the normativeconcept of health can be applied whether toindividuals (e.g., in maintaining proper cholesterolor blood sugar levels) or ecosystems (RAPPORT, 1989b;EHRENFELD, 1993; HOLLING & MEFFE, 1996) byimplementing the concept of evaluation withregard to normal variation (KING, 1993). Just asprocesses within individuals (e.g., metabolism,digestion, respiration) are important to manage-ment in this regard, so are the processes withinthe higher levels of biological organization, suchas nutrient flow in ecosystems (e.g., HOLLING &MEFFE, 1996). Other ecosystem features that aresubject to limited natural variation include numbersof species, trophic structure, energy storage,population variation and total biomass levels.

    How are the goals and standards from centraltendencies of use? Such information can be usedto evaluate both human and nonhuman systems.What happens if the characteristics of anecosystem are outside the normal range of naturalvariation? Direct management of ecosystems isimpossible because of the lack of control overecosystems (EHRENFELD, 1981; MCNEILL, 1989; HOLLING& MEFFE, 1996; MANGEL et al., 1996; COMMITTEE ONECOSYSTEM MANAGEMENT FOR SUSTAINABLE MARINEFISHERIES, 1999; FRANCIS et al., 1999). That is,management cannot be carried out to avoid manyof the effects of attempted control (whether it becontrol of other individuals, species ecosystems,or the biosphere); many such consequences areunintentional and unpredicted. However,, humansdo influence ecosystems, as do all species. Bothpast and present human influence has resulted inecosystems that exhibit abnormal qualities, butinfluence is something that every species has.Human influence may be interpreted as a limitedform of control over ecosystems, but managementcan not control the fact that there will beunintended consequences (ROHMAN, 1999) as theside effects of influence. This lack of control isone of the limitations that is experienced inmanagement in general. It is impossible to exertinfluence and, at the same time, know or controlall of the effects. In part, the lack of control stemsfrom being a part of ecosystems humans arecomponents (and the human species is acomponent, tenet 9, appendix 1) subject to thecollective limits described above (BATESON, 1972;ONEILL et al., 1986; KOESTLER, 1987; ONEILL et al.,1986; SALTHE, 1985; WILBER, 1995).

    So where do the central tendencies havepractical application? How can management usesuch information in view of the fact that allinfluences lead to secondary (or other higherorder) effects, at least some of which will resultin feedback over various scales of time thatplaces (or will place) limits on humans? The 8thtenet of management (appendix 1) is based onthe fact that the elements over which there ismost control are the human elements, recogniz-ing that even in self control there will be

    ramifications in the rest of the systems of whichhumans are a part. Some of these effects will bedesirable from certain points of view, but otherswill be negative (that is, many of the effects ofmanagement action will result in feedback thatwill have limiting effects on individual humansand our species). All effects would be positive ifmanagers had full control, but it is humanlyimpossible to control or predict which will bebeneficial and which will not (WOOD, 1994). Eventaking mitigating action to avoid influencesbeyond those intended will always have itsunintended consequences. There is one remainingalternative. It is the option of exerting self control(intransitive or passive management in whichhumans regulate what humans do, MCCORMICK,1999). To exercise this option humans doeverything possible so that humans fall withinthe normal range of natural variation, guided bycentral tendencies.

    This is a critical point. What it means tomanagement is: humans undertake change to exertinfluence and exhibit characteristics so as to be apart of biological systems in which humans fallwithin the normal range of natural variation(DARWIN, 1953; OVINGTON, 1975; PICKETT et al., 1992;FUENTES, 1993; MCNEILL, 1993; GRUMBINE, 1994b;MOOTE et al., 1994; SALZMAN, 1994; WOOD, 1994;MANGEL et al., 1996; CLARK, 1989; UHL et al., 2000).As suggested by APOLLONIO (1994), humans havethe alternative of mimicking other species. Otherspecies serve as empirical examples of sustainability.Mimicking can be accomplished by ensuring thathumans fall within the normal range of naturalvariation (especially in finding positions near centraltendencies as standards of reference, ormanagement guidelines, FOWLER et al., 1999). Thisamounts to an extension of biomimicry (BENYUS,1997) to the species level to address not onlyquestions about how to feed ourselves, but alsohow many humans there should there be to feed.Alternatively it can be viewed as parallel to theprocess of benchmarking in business management(SPENDOLINI, 1992; BOGAN & ENGLISH, 1994; BOXWELL,1994; CAMP, 1995), with hierarchical options. First,managers can find the advisable constraints onwhat businesses are and do (as in conventionalbenchmarking), and secondly, managers can addressthe metalevel question of whether or not anyparticular business should even exist, and if so atwhat level they carry out their functions andinfluence. It is an application of restoration ecologyto restore human involvement in nature so as tofall within the normal range of natural variation.Nature has been carrying out a form of adaptivemanagement (HOLLING, 1978; WALTERS & HILBORN,1978; WALTERS, 1986) over evolutionary time scalesso that it is now possible to take advantage ofeons of natural experiments with sample sizesinvolving millions of trials. In short, it is possible tolearn from nature (GRUMBINE, 1994b), or learn tolive as humans by observing other species, much inline with the philosophy of Thoreau and Muir

  • Animal Biodiversity and Conservation 25.2 (2002) 19

    (who saw ...sensitive observation of nature as thesource of wisdom, NORTON, 1994), or Leopoldwho pointed out that wilderness provides a basedatum of normality (CHRISTENSEN et al., 1996).

    The degree to which current forms ofmanagement are transitive varies. Terrestrialsystems are often more engineered in agriculturalpractices than are marine systems (however,aquaculture is quite transitive in this regard).Most fisheries are managed by controlling thefishing effort; nevertheless fish populations aretransitively driven to predetermined levels to elicitdesired productivity without serious or exhaustiveconsideration of the systemic consequences. Nosuch transitive management has withstood thetest of evolutionary time scales and suchapproaches fail to acknowledge the track recordof human failure in similar circumstances interrestrial settings (e.g., PONTING, 1991).

    Regardless of context, however, what is beingdone in most of current management ignoreslimits as they apply to humans. Management failsto place humans within the normal range ofnatural variation in conventional approaches afact that is often mentioned in the literature onmanagement and especially in literature criticalof conventional management practices (e.g.,GADGIL & BERKES, 1991). This point is maderepeatedly in work that draws empiricalinformation produced in scientific studies to theattention of society, particularly managers.Shortcomings and failures are most clear withregard to management at the ecosystem levelwhere the need for changes and alternatives areemphasized (e.G., AGEE & JOHNSON, 1988a).However, among scientists, the full importance oflimits is not always recognized (GRUBB, 1989).Socially, freedom is often confused with ignoringthe laws of nature (JOHNSTON, 1991). PIANKA (1974)sees a generic pattern in human failure to see thewisdom of finding a place (balance) betweenupper and lower limits. Many of the worldsproblems today can be attributed to the lack ofthis mode of management (WOODWELL, 1990).Continuing to ignore limits is no longer a tenableoption (CLARK, 1989; MANGEL et al., 1996; NATIONALMARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLESADVISORY PANEL, 1998). It is of paramountimportance to find a place for humans within thenormal limits of natural variation. As will be seenlater in this paper, there are many cases wherehumans are so far outside the normal range ofnatural variation that other elements of biologicalsystems have responded to show abnormalvariation themselves (CHRSITENSEN et al., 1996). Inthe end, there is really no choice but that offinding the human place within the limits of thesystems of which humans are a part (MCNEILL,1993). The effects already caused by the cases ofhuman abnormality, or pathology, continue tounfold through delayed consequences. Hopefullythese are not so extreme as to preclude otherwiseviable options for management. The risks resulting

    from past actions are risks that are yet to befaced (OVINGTON, 1975) and the remaining hope isthat actions taken now will both avoid furtherrisk as well as reduce risk from past mismanage-ment. One of the challenges will be to conductresearch that provides needed information (ORIANS,1990; KATES et al., 2001, tenets 5 and 6,appendix 1). This clearly includes demonstrationof the central tendencies of natural variation,and displaying them in graphic form (FOWLER &PEREZ, 1999). These central tendencies occurbetween limits. As maintained by CLARK (1989),one of the main functions of scientific endeavor isthe production of information about limits theybound the central tendencies and present managerswith viable options to address one of the mainquestions of sustainability science (as quoted inthe introduction, KATES et al., 2001).

    Discussion: systemic management, a movein the right direction

    What happens if management follows theguidelines established to avoid the problemscreated by current approaches? The various tenetsof management in appendix 1 have been developedover the last several decades in trying to solvemanagement problems (e.g., CHRISTENSEN et al.,1996; MANGEL et al., 1996; NATIONAL MARINE FISHERIESSERVICE ECOSYSTEM PRINCIPLES AAVISORY PANEL, 1998;UNITED STATES INTERAGENCY ECOSYSTEM MANAGEMENTTASK FORCE, 1995; COMMITTEE ON ECOSYSTEMMANAGEMENT FOR SUSTAINABLE MARINE FISHERIES, 1999;MCCORMICK, 1999). Can management adhere tothem? Is it possible to avoid exacerbating problemsinherited from past actions while expanding thescope of management? Is it possible to includeecosystems or the biosphere without giving up onspecies or individuals as important levels ofbiological organization to which managementapplies? The implementation of systemicmanagement will lead toward accomplishingthese objectives (even if there is no guaranteethat future problems from the failures of pastmanagement can be avoided). It is a form ofmanagement that emerges from past practicesand draws on the lessons learned fromexperience. As stated at the outset, it embodiesthe principles that have emerged from concertedeffort to deal with problems that have not beenavoided in traditional management. Thefollowing sections provide more depth to thedefinition of systemic management.

    There is progress toward systemic managementseen in some of the conclusions reached inattempts to develop management at theecosystem level (ecosystem management). Oneconclusion is particularly important. As reviewedabove, it is not possible to manage ecosystems,but, at the same time, it is imperative thatecosystems be taken into account along withthe rest of complexity (especially in managing

  • 20 Fowler & Hobbs

    human interactions with various biotic systems).It is important that management proceed in waysthat apply, not only at the ecosystem level, butalso at the levels of individual, species, and thebiosphere. Singlespecies approaches should notbe abandoned to focus on ecosystems, or viseversa. How are such multiple goals accomplishedby systemic management? How can managementdeal with the fact that the forces and process ofindividuals, populations, species, ecosystems andthe biosphere are often in opposition (e.g., WILSON& SOBER, 1989; WILLIAMS, 1992)? Highly trainedand experienced specialists are often at odds witheach other based on conflicting interpretations inconventional management, in part because ofthe many opposing forces of nature. How doesadopting the principle of confining variation towithin its normal limits lead to adhering to thetenets of management, one of which requiresthat such issues be dealt with consistently (e.g.,across disciplines)?

    Limits to management options

    There are limitations on the options formanagement, consistent with there beinglimitations on everything. This is seen in theapplication of the tenets of management. Suchlimits lead to the elimination of many manage-ment options. Applying these limits is a processthat helps focus on what is possible and avoidsthe waste and problems created by trying thingsthat will not work. Within the full, or unlimited,suite of options are those that involve controllingnonhuman species, ecosystems, or the biosphere,as often attempted in the past. Attempts havebeen made, and more might be undertaken, todirectly control these systems without fullyconsidering the effects, especially those that resultin risks particularly to humans, and particularlyin the long run. However, it is increasingly clearthat these options can no longer be considered(tenet 8, appendix 1 and 2, and as concluded inthe literature referred to above) because, in eachand every case, there are always uncontrollableside effects that are systemic in nature somewith negative consequences for ourselves (e.g.,through the effects on the human environmentthat result in problems such as emergent diseases,RAPPORT & WHITFORD, 1999, or loss of resources).There are unintended consequences (negative orpositive, ROHMAN, 1999) to every managementaction. They may involve humans directly as parti-cipants in various systems, or indirectly througheffects on other members of such systems (whetherindividuals, species, ecosystems). It is impossible tocontrol the fact that such things happen. Thisleaves only options involving the control of humanactivities and the regulation of human influence(e.g., fish can not be regulated but commercialfishing can). By taking this approach, managementinvolves finding appropriate levels of influence byhumans (complete with all of their ramifications,

    positive or negative). Management can, forexample, proceed by addressing appropriate levelsof biomass consumption, whether from a speciesor an ecosystem, the numbers of species used asresources, or the extent o