Ecologia General Guia TP 2016 parte 2
Transcripción
Ecologia General Guia TP 2016 parte 2
Departamento Ecología, Genética y Evolución Guía de Trabajos Prácticos - Parte II Primer Cuatrimestre 2016 Ecología General ECOLOGÍA GENERAL – Primer Cuatrimestre 2016 http://www.ege.fcen.uba.ar/materias/general/general.htm DOCENTES Nombre E-mail Prof. Cecere, Carla [email protected] Prof "Pedro Flombaum [email protected] JTP Gustavo Thompson [email protected] JTP Diana Rubel [email protected] JTP Sebastián Torrela [email protected] Ayudante Primera Verónica Loetti [email protected] Ayudante Primera Rosario Lovera [email protected] Ayudante Primera Carolina Guerra [email protected] Ayudante Segunda Pedro Montini [email protected] Ayudante Segunda Samanta Thais Efron [email protected] Ayudante Segunda laura Calfayán Teóricas Trabajos Prácticos [email protected] Día Martes Viernes Miércoles y viernes Martes y jueves Miércoles y viernes Horario 18 a 21 14 a 17 9 a 13 (G. Thompson) 13:30 a 17:30 (D. Rubel) 17:30 a 21:30 (S. Torrela) Lista de Alumnos EGE: es una lista de distribución de información para alumnos del Departamento de Ecología, Genética y Evolución, acerca de becas, cursos y otras cuestiones de interés. No es una lista de discusión. Puede Ud. suscribirse a la lista en: http://www.ege.fcen.uba.ar/mailman/listinfo/alumnos o accediendo desde el link en la página del Departamento. También en esta página encontrará los correos electrónicos de los representantes estudiantiles del EGE, para realizar cualquier consulta. 2 Ecología General REGIMEN DE APROBACIÓN DEL CURSO Los requisitos para aprobar los trabajos prácticos son: (1) Aprobar 2 exámenes parciales con un mínimo de 60 puntos. Se podrán recuperar los 2 exámenes parciales. La fecha de recuperación será a posteriori del segundo examen parcial. A los fines de calcular la nota final de la materia se considerarán las notas de todos los exámenes. (2) Aprobar el 80% de los informes de los trabajos prácticos. El informe deberá entregarse la semana siguiente a la finalización del trabajo práctico. En caso de no ser aceptado será devuelto para su corrección y nueva entrega. En caso de no ser aceptado luego de la segunda corrección se considerará desaprobado. (3) Asistir al 80% de los trabajos prácticos. Se tomará asistencia al comienzo del trabajo práctico. Los alumnos que lleguen 10 minutos después de iniciado el mismo tendrán media inasistencia y los que lleguen luego de 20 minutos tendrán ausente. Los requisitos para aprobar la materia por promoción sin dar examen final son: (1) Aprobar los 2 exámenes parciales (sin la opción del recuperatorio) con un mínimo de 70 puntos cada uno y tener un promedio mínimo en los parciales de 80 puntos. (2) Aprobar todos los informes de los trabajos prácticos. (3) Tener los finales aprobados de las materias correlativas. La nota final para aquellos alumnos que hayan promovido será elaborada en base al promedio de los 2 exámenes parciales, los informes de laboratorio y el desempeño en Trabajos Prácticos. Aquellos alumnos que hayan aprobado los trabajos prácticos pero que no hayan promovido deberán dar un examen final escrito, cuya nota de aprobación es de 60/100 PROGRAMA ANALÍTICO INTRODUCCIÓN A LA ECOLOGÍA ¿Qué es ecología? Niveles de organización. Método científico en ecología. Nociones generales de biología evolutiva. Métodos de muestreo y diseño de experimentos en ecología. Escalas espaciales y temporales. Problemas ecológicos actuales. FACTORES QUE LIMITAN LA DISTRIBUCIÓN DE LOS ORGANISMOS Recursos y condiciones. Temperatura. Salinidad. Radiación. CO2. H2O. Nutrientes. Espacio. Ectotermos y endotermos. Nicho ecológico. Aclimatación, migración, almacenamiento y letargo. Principales recursos para plantas y animales. Generalistas, especialistas, oportunistas y selectivos. Biomas. POBLACIONES Concepto de población. Atributos poblacionales. Composición de la población. Abundancia y rango de distribución, tamaño corporal y latitud. Densidad absoluta y relativa e índices de densidad. Censos. Curvas poblacionales. Métodos basados en marcado y recaptura y en la reducción del tamaño poblacional. Disposición espacial: al azar, regular y contagiosa. Distribución de Poisson y Binomial negativa. Demografía. Estadística vital. Tablas de vida y de fecundidad. Curvas de supervivencia. Tasas de reproducción, tiempo generacional y tasas de incremento. Distribución de edades. Valor reproductivo. Poblaciones con generaciones discretas y con solapamiento. Historias de vida. Plasticidad fenotípica. 3 Ecología General Esfuerzo reproductivo. Edad de la primera reproducción. Iteroparidad y semelparidad. Tamaño y número de crías. Senescencia. Dinámica poblacional. Densodependencia y densoindependencia. Competencia intraespecífica. Curvas exponencial y logística: teoría y ejemplos de poblaciones naturales y de laboratorio. Modelos que incorporan un retraso temporal. Regulación poblacional. Demografía humana. Relaciones interespecíficas. Distintos tipos. Competencia interespecífica. Modelo de Lotka y Volterra. Concepto de nicho y principio de exclusión competitiva. Efectos de los predadores sobre la población de presas. Ciclos predador-presa: hipótesis sobre sus causas. Modelo de Lotka-Volterra y derivados. Parasitismo: Micro y macroparásitos. Infección y enfermedad. Transmisión y distribución. Efecto del parasitismo sobre el hospedador individual y su población. Herbivoría. Relaciones positivas entre especies: comensalismo, simbiosis. Coevolución. ESTRUCTURA Y DESARROLLO DE LA COMUNIDAD Características de la comunidad. Clasificación y ordenación de las comunidades. Descripción de la composición de la comunidad. Indices de diversidad. Análisis de gradientes. Comunidad clímax. Mecanismos del proceso de sucesión. Organización de la comunidad. Influencia de la competencia y predación en la estructura de la comunidad. Cadenas alimenticias y niveles tróficos. Especies principales y especies dominantes. Control "top-down" y "bottom-up" de las tramas tróficas. Gremios. Estabilidad de la comunidad. Dinámica temporal de las comunidades: concepto de sucesión. Sucesión primaria y secundaria. Tipos de sucesión. Determinantes de la biodiversidad. Efectos del clima, heterogeneidad espacial y temporal, perturbaciones, productividad. FLUJO DE ENERGÍA Y MATERIA A TRAVÉS DEL ECOSISTEMA Flujo de energía y materia a través del ecosistema. Redes y cadenas tróficas. Productividad primaria. Productividad secundaria. Eficiencias de transferencia de energía entre niveles tróficos. ¿Qué limita el número de niveles tróficos? Factores que limitan la productividad primaria en ecosistemas terrestres y acuáticos. Factores que limitan la productividad secundaria en ecosistemas terrestres y acuáticos. Ciclos biogeoquímicos. Alteraciones de los principales ciclos biogeoquímicos. ECOLOGÍA DE PAISAJES Y REGIONES Desarrollo histórico. Conceptos de paisaje, región y ecosistema local. Modelo de parche-corredormatriz. Mosaicos y gradientes. Patrones espaciales. Teoría jerárquica. APLICACIONES DE LA ECOLOGÍA DE POBLACIONES Manejo y explotación de recursos naturales. Rendimientos máximo sostenible. Modelos de explotación. Rendimiento económico óptimo. Declinación de la abundancia de ballenas y otros ”stocks” pesqueros. Control de plagas y malezas: control biológico, cultural, genético y químico. Manejo integrado de plagas. Pesticidas: efectos adversos y positivos sobre la plaga y otros organismos. Nivel de daño económico y de umbral de acciones. BIODIVERSIDAD Y CONSERVACIÓN Concepto de biodiversidad. Valor intrínseco y utilitario de la biodiversidad. ¿Cuántas especies existen? Patrones geográficos de distribución de especies. Relaciones especies-area. Biogeografía de islas y modelo del equilibrio. Biodiversidad y estabilidad de los ecosistemas. Tasas de extinción históricas y recientes. Principales causas de extinciones recientes. Poblaciones viables mínimas. Conservación de especies amenazadas. Fragmentación del hábitat y efecto de borde. Diseño de reservas. CONTAMINACIÓN EN ECOSISTEMAS ACUÁTICOS Y TERRESTRES Tipos principales de contaminantes en el ambiente: orígenes y fuentes de emisión, ingreso y dinámica en el ambiente. Niveles ecológicos de acción. Bioconcentración y biomagnificación. Evaluación y diagnóstico de la contaminación: parámetros físicos y químicos de referencia. Bioindicadores. 4 Ecología General Respuesta de la biota al estrés ambiental. Indices ecológicos para cuantificar el deterioro ambiental. Bioensayos. Bibliografía Begon M, Harper JL y Townsend CR (1996) Ecology: individuals, populations and communities. Blackwell Sci., Oxford (Versión en español de la 2da. edición inglesa: (1990), Ed. Omega, Barcelona). Caughley G (1977) Analysis of vertebrate populations. Wiley, New York. Dobson AP (1996) Conservation and biodiversity. Scientific American Library, New York. Forman RTT (1995) Land mosaics. The ecology of landscapes and regions. Cambridge Univ. Press, Cambridge. Krebs CJ (1989) Ecological methodology. Harper Collins, New York. Krebs CJ (1994) Ecology: the experimental analysis of distribution and abundance. Harper Collins, New York (Versión en español de la 3ra. edición inglesa: (1985), Ed. Pirámide, Madrid). Rabinovich JR (1980) Introducción a la ecología de las poblaciones animales. CECSA, Caracas. Ricklefs RE (1997) The economy of nature. W. Freeman & Co., New York (Versión en español: Invitación a la ecología. Ed. Médica Panamericana, Buenos Aires). Smith, R. & Smith, T (2001) Ecología. 4ta. edición. Addison – Wesley. Madrid. Stiling PD (1996) Ecology: theory and applications. Prentice Hall, New Jersey. Townsend CR, Harper JL y Begon M (2000) Essentials of ecology. Blackwell Sci., Oxford.* 5 Ecología General ECOLOGIA GENERAL 2016 (1° Cuatrimestre). Cronograma ECOLOGIA GENERAL 2016 (1° Cuatrimestre). CRONOGRAMA Trabajos Prácticos DÍA FECHA Ma 15-mar Vier 18-mar TRABAJOS PRÁCTICOS Ma 22/23mar (LABO) -Inscripción/presentación -Actividad noticias. -Diseño experimental. Hipótesis y predicciones -Explicación TP Recursos y Condiciones e inicio de trabajo experimental con Lemnas Ju/Vier 24/25-mar FERIADO Ma 29/30mar (LABO + AULA) -Recuento de Lemnas (Semana 1). -Abundancia I: problemas, actividades de discusión -Introducción las áreas de estudio (Magdalena) -Muestreo: conceptos generales, técnicas (bosque/sotobosque) -Explicación/planificación de la salida campo Magdalena Vier 1-abr Salida a la Reserva de Magdalena Ma 5/6-abr (LABO + AULA) -Recuento de Lemnas (Semana 2). -TP Abundancia II: técnicas II (animales) -Explicación/planificación de la salida campo RECN -Informe científico, actividades y Guía TP. Vier 7/8-abr Salida de campo a la RECN Ma 12/13-abr Vier 14/15-abr Ma 19/20-abr Vier 22-abr Ma Vier (LABO + COMPU) -Recuento de Lemnas (Semana 3) -Análisis datos de la salida de campo: armado de base de datos (MAGDALENA) (COMPU) -Análisis datos de la salida de campo 2: vegetación, matecitos (LABO+COMPU) -Recuento de Lemnas (Semana 4). -Crecimiento poblacional: actividad sobre ideas previas, modelos, simulación, problemas Salida de campo San Vicente (a confirmar) (COMPU) -Crecimiento poblacional: fin problemas -Tablas de vida I (explicación-ejercicios). (COMPU) 28/29- abr -Tablas de vida II (ratones). -Cierre Lemnas. 26/27-abr 6 ECOLOGIA GENERAL 2016 (1° Cuatrimestre). Cronograma ECOLOGIA GENERAL 2016 (1° Cuatrimestre). CRONOGRAMA Trabajos Prácticos DIA FECHA Ma 17/18may Vier 20may Ma 24/25may Vier 26/27may Ma 31/1jun Vier 2/3-jun Ma 7/8-jun TRABAJO PRACTICO (LABO/AULA) REPASO (COMPU) (AULA) PARCIAL POR EL FERIADO del MIERCOLES 25 de mayo (LABO/AULA) -Atributos de las comunidades (Definiciones, Área Mínima, Diversidad e Índice Similitud). (LABO/AULA) -Atributos de las comunidades (cierre ejercicios Guia TP - Costanera Sur), - Invasiones Biológicas I: Seminario (COMPU) -Invasiones Biológicas II: parte I: TP ardillas (COMPU) -Invasiones Biológicas II: parte II: finalización + discusión de video -Análisis resultados avistaje de aves RECN Vier 9/10jun Ma 14/15-jun Vier 16/17-jun Ma 21/22-jun Vier Ma Vier Lu juev 23/24-jun 28-jun 1-jul 4-jul 7 julio (COMPU) -Ecología del Paisaje: Escalas + Gradiente urbano rural (GoogleEarth) (COMPU) -Cierre Eco de paisaje -Cambio Climático (actividad ciclo carbono) ( AULA) -Cierre Cambio Climático (video y discusión (AULA) -Actividad sobre producciones escritas de la salida Magdalena (informe). -Actividad Evaluación (Preguntas de Magdalena) (AULA) REPASO SEGUNDO PARCIAL Entrega notas 2º parcial Recuperatorio 1º parcial Recuperatorio 2º parcial Ecología General Seguridad en laboratorios de docencia ( 8 Ecología General 9 Ecología General 10 Ecología General 11 Ecología General 12 Ecología General 13 Ecología General ÍNDICE GENERAL DE TRABAJOS PRÀCTICOS – Parte 2 7. ATRIBUTOS DE LAS COMUNIDADES (1) Introducción (2) Guía de trabajo 8. SEMINARIO INVASIONES BIÓLOGICAS 9. INVASIONES BIOLÓGICAS (1) Introducción (2) Actividades 10. ECOLOGIA DEL PAISAJE (1) Introducción (2) Actividades 14 Ecología General Trabajo práctico 7 ATRIBUTOS DE LAS COMUNIDADES INTRODUCCIÓN En los libros de texto de ecología se pueden encontrar varias definiciones de “comunidad”, que cubren un rango considerable de significados. Algunos consideran a la comunidad como “un ensamble de poblaciones de plantas, animales, bacterias y hongos que viven en un ambiente y que interactúan unos con otros, formando juntos un sistema viviente distintivo con su propia composición, estructura, relaciones ambientales, desarrollo y función” (Whittaker 1975). En el otro extremo, se la ha considerado como “cualquier conjunto de organismos que viven cerca unos de otros y acerca de los cuales es interesante hablar” (MacArthur 1971). Todas las definiciones, no obstante, concuerdan en que las comunidades son conjuntos de individuos de distintas especies que aparecen juntos en tiempo y espacio, y la mayoría destaca la importancia de las interacciones entre esas poblaciones. Varios autores, por otra parte, señalan la existencia de propiedades emergentes de las comunidades, atributos de estructura (e.g., la composición de especies) o de funcionamiento (e.g., el flujo de energía) que son característicos de este nivel de organización. En alguna medida, las diferentes definiciones de comunidad son consecuencia de los distintos objetivos de los investigadores que las propusieron. Los ecólogos de plantas, que tratan con ensambles espacialmente fijos, a menudo enfatizan la descripción de tales asociaciones y sus cambios en el tiempo; los ecólogos de animales, confrontados con organismos móviles y activos, le dan más importancia a las interacciones y a las relaciones funcionales entre las especies. Algunos definen a la comunidad en términos de unidades de hábitat (e.g., las comunidades del intermareal), otros por categorías de formas de vida (e.g., comunidades herbáceas) o por taxonomía (e.g., comunidades de aves). Lo común a todas estas formas de definir a una comunidad es su valor operativo: todas se centran en una parte del conjunto total de especies que coexisten, pues es prácticamente imposible trabajar con el concepto original de comunidad (i.e., el conjunto de todos los individuos de todas las especies que viven en un determinado lugar). Es muy claro que la noción de comunidad, aún cuando se utilicen solo formas “operativas”, ha contribuido notablemente al desarrollo de nuestro entendimiento de la naturaleza (Wiens 1989). Los atributos comunitarios más comúnmente utilizados por los ecólogos son los siguientes: • Diversidad específica: es una función de la riqueza específica (número de especies presentes) y de la equitatividad (grado de uniformidad de las abundancias relativas de las especies). La variación conjunta de ambos componentes determina los cambios en la diversidad. • Dominancia: no todas las especies tienen la misma influencia sobre la comunidad; las dominantes pueden ejercer un mayor control sobre la estructura comunitaria. La dominancia puede estar dada por su abundancia, tamaño o actividad. • Abundancia relativa: las abundancias relativas entre las distintas especies también permiten describir a las comunidades. • Estructura trófica: las relaciones alimentarias entre las especies de la comunidad determinan el flujo de materia y energía. • Interacciones entre especies: una de las ideas implícitas en el concepto de comunidad es que existen determinadas asociaciones de especies (i.e., que éstas aparecen juntas más a menudo que lo que uno esperaría por azar). Estas asociaciones pueden deberse a las interacciones entre ellas, como en el caso de las mutualistas, o ser consecuencia de afinidades de su biología (e.g., requerimientos de hábitat similares). 15 Ecología General De estos atributos comunitarios, uno de los más estudiados históricamente por los ecólogos ha sido la diversidad. El concepto de diversidad ha provisto un marco teórico importante para el desarrollo de muchas especulaciones acerca de la estructura y el funcionamiento de las comunidades (Magurran 1988). Al mismo tiempo, el interés por este tema se ha incrementado debido a la creciente necesidad de comprender los factores que gobiernan los patrones globales de biodiversidad (Sala et al. 2000). OBJETIVOS El objetivo general del trabajo práctico es familiarizarse con el cálculo de algunos atributos comunitarios, con algunos aspectos del muestreo de comunidades y con la determinación de la diversidad y sus componentes. Los objetivos específicos son: (1) Determinar el área mínima necesaria para estimar la riqueza específica de una comunidad. (2) Calcular la riqueza específica, la diversidad y la equitatividad de una comunidad. (3) Construir una curva rango-abundancia para una comunidad. (4) Evaluar el grado de similitud entre distintas comunidades. (5) Estimar similitudes y diferencias en los patrones de diversidad de varias comunidades y explorar las posibles causas. DESARROLLO Se utilizará un “mapa” de una comunidad imaginaria (ensamblar las cuatro hojas grilladas para obtener el “mapa”) . En el mapa se encuentran indicados (con distintas letras) los individuos de las distintas especies. El grillado facilita el muestreo, al mismo tiempo que cada cuadrado constituye una unidad muestreal mínima. 1.- Determinación del área mínima y de la riqueza específica de la comunidad Para evaluar el área mínima de muestreo necesaria para estimar la riqueza de la comunidad hay que realizar muestreos sucesivos de la riqueza en unidades de tamaño cada vez mayor (véase figura 1). En cada paso se duplica la superficie de muestreo, extendiendo la unidad anterior (Matteucci y Colma 1982). Las unidades muestrales sucesivas son: un cuadrado, dos cuadrados, cuatro cuadrados (2x2), ocho cuadrados, 16 cuadrados (4x4), 32 cuadrados, 64 cuadrados (8x8), etc. Comenzar el muestreo en alguna de las esquinas del borde izquierdo del mapa. Graficar el número de especies en función del tamaño del cuadrado. ¿Cuál es el tamaño que usted emplearía para determinar la riqueza de la comunidad y por qué? Examine cómo se modifica su resultado si hubiera comenzado el muestreo en alguna de las esquinas del borde derecho del mapa. ¿A qué lo atribuye? ¿Qué implicancias tiene esto para el muestreo de comunidades? 16 Ecología General Figura 1: Tamaños sucesivos de muestreador para la evaluación del área mínima. 57 58 59 60 61 62 63 64 49 50 51 52 53 54 55 56 41 42 43 44 45 46 47 48 33 34 35 36 37 38 39 40 25 26 27 28 29 30 31 32 17 18 19 20 21 22 23 24 9 10 11 12 13 14 15 16 1 2 3 4 5 6 7 8 2.- Estimación de la diversidad y de la equitatividad Para la diversidad, se utilizarán el índice de Shannon-Wiener (H) y el de Simpson (D). Utilizando un muestreador de 8 x 8, tomar 10 muestras al azar (elegir coordenadas x e y al azar, y colocar el extremo superior izquierdo del cuadrado muestral sobre la celda correspondiente; descartar el punto si no cabe el muestreador entero). En cada uno de los 10 casos, contar el número de individuos de cada una de las especies presentes, completando la tabla 1. Tabla 1. Número de individuos de cada especie por muestra (M), y suma de abundancias para cada especie. spp. A B C D E F G H I J K L M N M1 M2 M3 M4 M5 M6 M7 M8 M9 M10 Suma Sobre la base de la suma correspondientes a las 10 muestras, calcular los siguientes índices, utilizando la tabla 2: 17 Ecología General (a) Índice de Shannon-Wiener. Basado en la teoría de la información, predice cuál es la probabilidad de que un individuo en una muestra sea de la misma especie que el de la muestra anterior. S H = - ∑ (pi)(ln pi) i=1 donde H = contenido de información de la muestra (diversidad); S = riqueza específica; pi = proporción de individuos de la especie i respecto al total de individuos. Varía entre un valor mínimo de 0 y un máximo que depende de la riqueza específica (véase más abajo). (b) Índice de Simpson. Basado en la teoría de probabilidades. ¿Cuál es la probabilidad de que dos individuos tomados al azar pertenezcan a una misma especie? Si pi es la proporción de individuos de la especie i respecto al total de individuos, entonces en una muestra de dos individuos, la probabilidad de que sean los dos de la misma especie es pi * pi , o sea pi2. Si se suman las probabilidades para todas las especies presentes, se obtiene el índice de Simpson: S D = 1 - ∑ (pi)2 i=1 Este índice otorga mayor peso a las especies abundantes que a las raras. Varía entre un valor mínimo de 0 (cuando todos los individuos pertenecen a la misma especie) y un máximo de (1 - 1/S) cuando los individuos se reparten equitativamente entre especies. (c) Equitatividad. El valor máximo de diversidad varía con el número de especies presentes. Usando el índice de Shannon-Wiener, para un S dado, el H será máximo cuando los individuos se distribuyan equitativamente entre las especies (i.e., cuando todos los pi sean iguales entre sí e iguales a 1/S). Reemplazando en la fórmula de H: S Hmáx = - ∑ (1/S)(ln 1/S) = - S(1/S)(ln(1/S)) = ln S i=1 Equitatividad = H/Hmáx = H/ln S Tabla 2. Valores utilizados para el cálculo de la diversidad y la equitatividad. ln pi (pi)(ln pi) (pi)2 Suma pi spp. A B C D E F G H I J K L M N ∑ 18 Ecología General 3.- Construcción de la curva de rango-abundancia Utilizando los datos de abundancia relativa (pi) de cada una de las especies (tabla 2), se debe ordenarlas en orden decreciente de abundancia, asignándole rango 1 a la más abundante, 2 a la segunda, y así sucesivamente. Volcar los datos de abundancia relativa en función del rango en la figura 2. Figura 2. Curva de rango-abundancia. Abundancia relativa (pi) Rango 4.- Estimación de la similitud entre comunidades Existen distintos índices que permiten comparar comunidades de a pares (Matteucci y Colma 1982, Crisci y López Armengol 1983). Estos índices pueden ser cualitativos o cuantitativos. Los primeros se basan solo en la presencia o ausencia de las distintas especies en las dos comunidades que se comparan, mientras que los cuantitativos utilizan información de la abundancia relativa de las especies. (a) Índice de Jaccard. Este índice cualitativo tiene en cuenta la relación entre el número de especies comunes a las dos comunidades que se comparan y el total de las especies en ambas comunidades. En la tabla 3 se muestra un esquema de los valores utilizados. Los valores oscilan entre 0 y 1. El índice es: Similitud = a / (a + b + c) (b) Índice de Sorensen. Este índice cualitativo concede mayor significación a las presencias conjuntas. Los valores oscilan entre 0 y 1. El índice es: Similitud = (2a) / (2a + b + c) Tabla 3. Esquema de los valores utilizados para calcular la similitud cualitativa entre dos comunidades A y B. En la tabla, a es el número de especies comunes a A y B, b es el número de especies exclusivas de B, c es el número de especies exclusivas de A, y d es el número de especies ausentes en ambas muestras simultáneamente. Comunidad B Presente Ausente Comunidad A Presente Ausente a b c d 19 Ecología General (c) Índice de Czekanowski. Este índice cuantitativo está basado en la menor abundancia de cada especie en las comunidades que se comparan. Los valores oscilan entre 0 y 1. El índice es: S Similitud = ∑ mín (pi1, pi2) i=1 donde pi1 = proporción de individuos de la especie i respecto al total de individuos en la comunidad 1; pi2 = proporción de individuos de la especie i respecto al total de individuos en la comunidad 2. Tabla 4. Abundancia de las especies de aves acuáticas en la Reserva Costanera Sur (C.S.) durante primavera, verano, otoño e invierno, y de las especies de aves acuáticas en humedales cercanos a Chascomús, Chasicó (al oeste de Bahía Blanca) y Mar Chiquita (en la costa, al norte de Mar del Plata). Los valores corresponden al número de individuos observados en censos estandarizados. spp. Podiceps rolland Podiceps major Phalacrocorax olivaceus Egretta thula Bubulcus ibis Plegadis chihi Coscoroba coscoroba Cynus melancoryphus Anas georgica Anas flavirostris Anas platalea Anas cyanoptera Anas versicolor Dendrocygna bicolor Dendrocygna viduata Netta peposaca Heteronetta atricapilla Oxyura vittata Rallus sanguinolentus Fulica rufifrons Fulica leucoptera Fulica armillata Gallinula chloropus Jacana jacana Himantopus melanurus Vanellus chilensis Larus maculipennis Larus dominicanus Sterna trudeaui Podiceps occipitalis Anas sibilatrix Anas bahamensis Aramus guarauna Charadrius falklandicus Zonibyx modestus Gelochelidon nilotica Tringa flavipes Charadrius collaris C.S. primav 140 69 29 25 27 19 25 10 12 9 8 9 15 2 14 32 23 1 25 125 168 18 7 6 5 1 1 7 5 C.S. verano C.S. otoño 3 1 1 2 1 5 17 20 12 1 26 145 58 10 38 25 20 C.S. inv 128 63 19 7 7 6 14 16 2 3 2 2 3 5 1 8 26 24 1 17 98 529 6 1 1 2 1 1 3 Chascomús Chasicó 322 28 43 12 7 25 21 32 11 32 12 8 25 13 5 31 16 45 6 44 65 426 35 12 9 4 14 2 124 155 198 1 3 1 12 5 18 12 5 23 11 2 1 15 2 15 2 21 3 Mar Chiquita 77 23 36 12 7 12 13 17 33 32 14 46 24 87 107 98 23 45 8 67 48 19 1 25 12 1 Ecología General En la tabla 4 se presentan datos correspondientes a las abundancias de especies de aves acuáticas en la Reserva Costanera Sur (Buenos Aires) en distintas épocas del ciclo anual y en otros humedales de la provincia de Buenos Aires. Usando dichos datos, calcule la similitud (con los tres índices descriptos arriba) entre la comunidad de aves acuáticas de Costanera Sur y las otras tres comunidades (para Costanera Sur utilice solamente los valores invernales, pues los datos de las comunidades de la provincia de Buenos Aires fueron tomados en dicha estación). Comparar los resultados obtenidos con los distintos índices. ¿Cuáles podrían ser las causas del grado de similitud observado entre las comunidades. 5.- Patrones de diversidad Los datos de Costanera Sur de la tabla 4 corresponden a cuatro períodos del ciclo anual, y fueron tomados en un año en el cual se produjo una inusual sequía. Los niveles de agua de las lagunas de la reserva (que dependen del régimen de precipitaciones y de las temperaturas) son máximos durante el invierno, y van disminuyendo hasta su mínimo durante el verano y el otoño subsiguiente. Durante el verano estudiado casi la totalidad de las lagunas estaban secas, dejando solo grandes extensiones barrosas. Para el otoño, aunque el nivel del agua era bajo, ya había una superficie anegada considerable. Calcular la diversidad (usando el índice de Shannon-Wiener), la riqueza de especies y la equitatividad correspondiente a los cuatro muestreos. Examine comparativamente los valores obtenidos. ¿De qué manera afectan la riqueza y la equitatividad a las estimaciones de diversidad? Construya la curva de rango-abundancia de cada muestreo. ¿Qué conclusiones puede alcanzar comparando las cuatro curvas? ¿Cómo se relaciona la forma de las curvas con los valores de diversidad y sus componentes? ¿Cuáles podrían ser las causas de los patrones observados? REFERENCIAS Crisci JV y López Armengol MF (1983) Introducción a la teoría y práctica de la taxonomía numérica. Monografía 26, Serie de Biología. OEA, Washington DC. MacArthur RH (1971) Patterns of terrestrial bird communities. Pp. 189-221 en: Avian biology. Farner DS y King JR (eds). Academic Press, New York. Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton. Matteucci SD y Colma A (1982) Metodología para el estudio de la vegetación. Monografía 22, Serie de Biología. OEA, Washington DC. Sala OE, Chapin III FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, LeRoy Poff N, Sykes MT, Walker BT, Walker M & Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770-1774. Whittaker RH (1975) Communities and ecosystems. Second edition. Macmillan, New York. Wiens JA (1989) The ecology of bird communities. Volume 1. Foundations and patterns. Cambridge University Press, Cambridge. 21 170 Opinion 45 Fowler, S.V. et al. (1996) Comparing the population dynamics of broom, Cytisus scoparius, as a native plant in the United Kingdom and France, and as an invasive alien weed in Australia and New Zealand. In Proceedings of the Ninth International Symposium of Biological Control of Weeds (Moran, V.C. and Hoffmann, J.H., eds), pp. 19–26, University of Cape Town 46 DeLoach, C.J. (1995) Progress and problems in introductory biological control of native weeds in the United States. In Proceedings of the Eighth International Symposium on Biological Control of Weeds (Delfosse, E.S. and Scott, R.R., eds), pp. 111–112, CSIRO Publishing 47 Hawkins, B.A. et al. (1999) Is the biological control of insects a natural phenomenon? Oikos 86, 493–506 TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 48 Hosking, J.R. (1995) The impact of seed- and podfeeding insects on Cytisus scoparius, In Proceedings of the Eighth International Symposium on Biological Control of Weeds (Delfosse, E.S. and Scott, R.R., eds), pp. 45–51, CSIRO Publishing 49 Straw, N.A. and Sheppard, A.W. (1995) The role of plant dispersion pattern in the success and failure of biological control. In Proceedings of the Eighth International Symposium on Biological Control of Weeds (Delfosse, E.S. and Scott, R.R., eds), pp. 161–168, CSIRO Publishing 50 Southwood, T.R.E. et al. (1982) The richness, abundance and biomass of the arthropod communities on trees. J. Anim. Ecol. 51, 635–649 51 MacFarlane, R.P. and van den Ende, H.J. (1995) Vine-feeding insects of old man’s beard (Clematis vitalba), in New Zealand. In Proceedings of the Community ecology theory as a framework for biological invasions Katriona Shea and Peter Chesson Community ecology theory can be used to understand biological invasions by applying recent niche concepts to alien species and the communities that they invade. These ideas lead to the concept of ‘niche opportunity’, which defines conditions that promote invasions in terms of resources, natural enemies, the physical environment, interactions between these factors, and the manner in which they vary in time and space. Niche opportunities vary naturally between communities but might be greatly increased by disruption of communities, especially if the original community members are less well adapted to the new conditions. Recent niche theory clarifies the prediction that low niche opportunities (invasion resistance) result from high species diversity. Conflicting empirical patterns of invasion resistance are potentially explained by covarying external factors. These various ideas derived from community ecology provide a predictive framework for invasion ecology. Katriona Shea* Dept of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park, PA 16802, USA. *e-mail: [email protected] Peter Chesson Section of Evolution and Ecology, University of California, Davis, CA 95616, USA. Biological invasions are having a major impact on the Earth’s ecosystems [1], giving urgency to a better understanding of the factors that affect them. Some recent reviews have considered invasions from a variety of viewpoints, including the characteristics of invaders [2], the characteristics of invaded communities [3], resources [4,5] and natural enemies [6]. As these issues are not independent, it is essential to find a means of considering them jointly. Towards this goal, a theoretical framework for invasion ecology based on community ecology theory is proposed here. We show how this framework applies to the analysis Eighth International Symposium on Biological Control of Weeds (Delfosse, E.S. and Scott, R.R., eds), pp. 57–58, CSIRO Publishing 52 Burki, C. and Nentwig, W. (1997) Comparison of herbivore insect communities of Heracleum sphondylium and H. mantegazziaum in Switzerland (Spermatophyta: Apiaceae). Entomol. Gen. 22, 147–155 53 Syrett, P. and Smith, L.A. (1998) The insect fauna of four weedy Hieracium (Asteraceae) species in New Zealand. New Zealand J. Zool. 25, 73–83 54 Hight, S.D. (1990) Available feeding niches in populations of Lythrum salicaria L. (purple loosestrife) in the northeastern United States. In Proceedings of the Seventh International Symposium on Biological Control of Weeds (Delfosse, E.S., ed.), pp. 269–278, Istituto Sperimentale per la Patologia Vegetale of the factors promoting invasion, and use it to examine correlations between invasion resistance and species diversity. Invasion involves two essential stages: transport of organisms to a new location [7,8]; and establishment and population increase in the invaded locality [9]. A third stage, applicable to the most worrisome invasions, is regional spread from initial successful populations [10]. We focus on the second stage, where community ecology theory has most to offer. There is much evidence that the chance of establishment increases markedly with the rate of arrival of an alien species at a potential invasion site [2]. However, for establishment and growth, a species must be able to increase in abundance at the invaded locality. This depends on the opportunities that the particular invaded community provides for the invader in question. Niches and niche opportunities Three main factors contribute to an invader’s growth rate: resources [4,5,11,12], natural enemies [7,13,14] and the physical environment [15,16], all of which vary in time and space. How a species responds to these factors, including their spatial and temporal variation, determines its ability to invade. Once an invader has achieved an appreciable density, it will have effects on the invaded locality – for example, by consuming resources and maintaining natural enemies. Such responses and effects are the two defining aspects of an organism’s niche, according to a recent definition (Box 1). The response aspect of the niche is fundamental to an alien species’ ability to invade, and the effect aspect is fundamental to the impact that the invader has in the invaded community (Box 2). Both effects and responses of resident species in a community determine whether that community provides opportunities for invasion – that is, whether it provides niche opportunities (Box 1). In simple circumstances, niche opportunities can reduce to either resource opportunities or natural enemy escape opportunities. http://tree.trends.com 0169-5347/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02429-6 Opinion TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 171 Box 1. Concepts and definitions Ecological niches are defined by the relationships between organisms and the physical and biological environment, taking into account both time and space. A particular combination of physical factors (e.g. temperature and moisture) and biological factors (e.g. food resources and natural enemies) at a particular point in time and space defines a point in niche space. A modern definition of a species’ ecological niche is the response that the species has to each point in niche space and the effect that the species has at each point [a]. Responses are defined in terms of demographic variables, such as survival and individual growth; but of most importance is the overall outcome of these responses, the per-capita rate of increase. Effects include consumption of resources, interference with access to resources by other organisms, support of natural enemies and occupancy of space. Organisms respond to resource availability [b], which is the density of unused resource in the environment – soil water content, for example. Resource supply [b] is the net rate at which resources enter the system, discounting use by the organisms present (for example, rainfall minus evaporation and runoff but not transpiration). Resource availability is the net resource result of the effects of all the organisms in a system and the supply of the resource. A resource opportunity is defined as a high availability of resources on which a potential invader depends. Resource opportunity includes the effects of mutualists, such as pollinators, because they provide services [c,d] that could also be considered resources. Similarly, a natural enemy escape opportunity is defined as a low level or low efficiency of natural enemies to which invaders might be susceptible. A niche opportunity is the potential provided by a given community for alien organisms to have a positive rate of increase from low density. This might occur because of a resource opportunity, an escape opportunity or because of some favorable combination of resources, natural enemies and physical environmental conditions, including their fluctuations in time and space (Fig. I). Low levels of niche opportunities lead to invasion resistance of a community – that is, few alien species are able to successfully invade the community. Maturity is the opportunity a system has had to accumulate species, and for adaptation to the system to have taken place. It depends on the time that the system has had the current climate, including its short-term fluctuations and recurring disturbance events. Maturity depends also on the size of the species pool that has historically served as a source of species to the system [e]. References a Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 b Tilman, D. (1982) Resource Competition and Community Structure, Princeton University Press Resource opportunities Resource opportunities arise when the resources that a species needs are high in availability. This is not simply because resources are supplied at a high rate, but also because the effects of resident species have not reduced resource densities [17–20] or interfered with access to resources too greatly [21]. In cases where a potential invader and a resident species are limited by a single resource, Tilman’s R* rule (where R is resource availability; Box 2) predicts that invasion will occur if the resident’s R* is greater than the invader’s R*. For example, invasion would result if the invader had a higher http://tree.trends.com Environment Specialist Generalist Enemy escape opportunities Invader Resource opportunities Resources Competitors TRENDS in Ecology & Evolution Fig. I. Main components of niche opportunity. Blue arrows are positive effects on the invader; red arrows are negative effects. Arrows from the outer boxes to the inner box represent direct effects of the community on the invader. Arrows between community components represent indirect effects on the invader, and they are colored according to their indirect effect on the invader, which is opposite to their direct effect on the community component. The environment directly affects all components and modifies their interactions with other components. Not shown are the effects of specialist natural enemies of community members. These specialists will limit community members and so have positive indirect effects on the invader. Sometimes generalists might not attack the invader, in which case their effects would be like those of specialists on community members. (Weevil photograph courtesy of CSIRO, Australia.) c Richardson, D.M. et al. (2000) Plant invasion – the role of mutualisms. Biol. Rev. 75, 63–93 d Mack, R. et al. (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10, 689–710 e Huston, M. (1994) Biological Diversity, Cambridge University Press resource acquisition rate than that of the resident species at the same resource densities (e.g. by having a superior foraging technique; Box 2 [11]). Invasion would also occur if the invader had a lower maintenance requirement than that of the resident (Box 2). Simple resource limitation might be approximated in the case of space or food competition of a species invading the habitat of a very similar species [11,22]. Invader success, however, is also predicted for the case of limitation by multiple resources [23], as long as the invader always has a higher response (per-capita growth) than the resident. Most importantly, these conclusions are 172 Opinion TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 Box 2. Resource competition ideas The per-capita growth rate of a population limited by a single resource is the net effect of the gain from consumption of the resource, and the losses due to metabolism, tissue death (e.g. leaf fall and herbivory) and death of individuals. Thus: 1 dN = af (R ) − m N dt (I) where N is population density, R is resource availability, af (R ) defines the gain (the response of the species to the resource), and m (the maintenance requirement) is the total of all losses. The gain consists of the two parts: the constant a defining the overall magnitude of the response to the resource and the function f (R ) defining how response to the resource changes with resource abundance. The dynamics of the resource are given by: dR = S (R ) − g (R )N dt (II) where S(R) is the supply rate of the resource, and g(R ) the per-capita effect of the species on the resource. Multiplying g(R ) by N gives the total effect of the species and determines the impact of the invader in the invaded community. Normally, there would be a unique value R * of R at which equilibrium would occur – that is, af (R *) = m. For an alien species to invade, it must have a smaller value of R * than does a resident at equilibrium with the resource, because this is the value of resource availability that the alien experiences when it arrives in the system. Only if the resident’s R * value exceeds that of the invader can the invader have a positive growth rate. This is Tilman’s R * rule [a]. An alien might have a smaller R * value by having a smaller maintenance requirement. Alternatively, it might have a higher response than a resident [i.e. a larger value of af (R )]. This might be achieved by taking up the resource at a faster rate or by being more efficient at converting that uptake into gain. Different responses for different species might be modeled by having a vary with the species. In this case, R * would be an increasing function of m/a, and an invader would be successful if it had a smaller value of m/a than that of a resident. Although this R * theory was originally developed as an equilibrium theory [a], in the form where species can differ in a or m, the theory is robust to fluctuations in R and m, with the result being that an alien having a mean of m/a smaller than that of a resident can invade [b]. See Box 3 for situations in which R * theory does not hold. References a Tilman, D. (1982) Resource Competition and Community Structure, Princeton University Press b Chesson, P. and Huntly, N. (1997) The roles of harsh and fluctuating conditions in the dynamics of ecological communities. Am. Nat. 150, 519–553 robust to environmental fluctuations [24] and are not restricted to strict equilibrium scenarios, even though the R* rule was first derived in that context (Box 2). Such uniform superiority of an invader would make it an invader of large effect, because it would depress or displace all resident species relying on the same resources, with the details of the invasion depending on the effect component of the invader’s niche (Box 2). More generally, an invader would not be uniformly superior to any resident species, but instead might have a superior response to a particular resource, certain abundances of resources, or resources found in certain places or times [25]. Any situations in which residents do not keep resources at uniformly low levels are a potential resource opportunity [4,5] (Box 3). In some situations, the effect aspect of a species’ niche can also have a role in its invasion. Where a species has spatially localized effects, as in the case of plants, it will potentially have a strong effect on a small spatial scale, benefiting itself more than other species. For example, allelopathic effects of an invader might reduce densities of other species, increasing resource availability to the invader [26]. http://tree.trends.com Also, some species generate disturbance or alter disturbance regimes, freeing resources and thereby facilitating their own and other invasions [4,27–29]. Natural enemy escape opportunities Escape opportunities arise when natural enemies, such as diseases, predators and parasites, are in low abundance or are less effective against new species [13,14]. Community ecology theory claims strong symmetries between the effects of natural enemies and the effects of resources on community dynamics [30–32]. Thus, parallel to the R* rule for resources, there is a P* rule for natural enemies (where P indicates predator, pathogen or parasite density). Responses to natural enemies include elevated mortality rates and reduced feeding rates, leading to lower per-capita growth rates. Effects of residents on natural enemy densities are parallel to the effects of resident species on resource availability. Although species can vary greatly in resource dependence, natural enemies vary greatly in their specificity [33]. An invader might not be affected by specialist natural enemies preexisting in the invaded community and might gain a considerable advantage because it leaves its own specialist natural enemies behind or loses them early in the invasion process while at too low a density to maintain them [13,14]. This potential forms the basis of biological control of invaders [7,8] (but see Keane and Crawley in this issue [6]). Generalist natural enemies of the invaded community, however, will have effects that vary with their ability to attack the invader [6]. A naive invader might not be well defended against these enemies, in which case they reduce the escape opportunity of that invader [34]. However, generalists of the invaded community might not be equipped to attack the invader, in which case they increase the invader’s escape opportunity [6]. Interactions between the physical environment, resources and natural enemies In some studies, there has been a strong emphasis on the physical environment as a constraint on invasions [15,16]. However, many species have broad environmental tolerances, and the interaction of environmental factors with resources and natural enemies has a potentially important role. For example, with plant species, higher temperatures could mean higher evaporative water loss, lower water-use efficiency and, therefore, higher demand for water as a resource [35]. Similarly, a harsh physical environment could lead to a higher maintenance requirement as a result of higher mortality, higher biomass attrition rates (in plants) or higher metabolic costs (Box 2). A harsher physical environment might therefore require higher resource availability to achieve the same capacity for increase. However, as both residents and invaders respond to environmental harshness, it is the difference in the response of the residents and invader that determines Opinion TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 Box 3. Resource opportunities in fluctuating environments Community ecology theory predicts that spatial and temporal environmental variation has an important role in species coexistence [a]. For invaders, this can mean spatial and temporal niche opportunities, provided that invaders and residents differ in their responses to varying factors. Most species have periods of relative activity and relative inactivity during a year [b]. Niche opportunities arise during times when resident species are relatively inactive and are not placing high demands on resources. Using the notation given in Box 2, the per-capita growth rate of a species might be represented as: 1 dN = a (t )f (R )− m N dt [I] with a now a function of time to represent temporally varying growth activity: it is the response of the organism to time. The theory of the storage effect [b] shows that a species can invade even if it has an average value of a(t ) less than that of resident species, provided that the invader’s a(t ) is sufficiently large compared with residents’ a(t )s some of the time; for example, the activities of the invader and residents might fluctuate out of phase. Fluctuations in a(t ) can be deterministic (e.g. seasonal) or stochastic (e.g. in response to yearly weather variation) [b,c]; the key feature is that the invader must show a different temporal pattern of response than that of the residents. An invader might also gain an advantage by responding differently to changes in resource levels than do residents – that is, by having a function f (R) that differs nonlinearly from that of residents [a,d]. For example, the invader might have a stronger response than residents at both high and low resource availabilities, but not at intermediate resource availabilities. Resource fluctuations between high and low values would then be a resource opportunity for the invader, a mechanism referred to as ‘relative nonlinearity of competition’ [a]. Spatial variation can also provide niche opportunities, and this can occur through spatial versions of the storage effect and relative nonlinearity of competition [e]. Much emphasized in the literature, however, are competition–colonization tradeoffs [f,g], which can work on a variety of scales. At the level of a local community, the mechanism can be driven by disturbance. In sessile communities, death of an individual is a substitute for disturbance. Most importantly, this mechanism means that an inferior competitor for resources could invade if it had superior colonization or local resource exploitation ability [g]. References a Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 b Chesson, P. et al. (2001) Environmental niches and ecosystem functioning. In Functional Consequences of Biodiversity (Kinzig, A. et al., eds), pp. 213–245, Princeton University Press c Lehman, C.L. and Tilman, D. (2000) Biodiversity, stability, and productivity in competitive communities. Am. Nat. 156, 513–552 d Armstrong, R.A. and McGehee, R. (1980) Competitive exclusion. Am. Nat. 115, 151–170 e Chesson, P. (2000) General theory of competitive coexistence in spatially-varying environments. Theor. Popul. Biol. 58, 211–237 f Tilman, D. (1994) Competition and biodiversity in spatially structured habitats. Ecology 75, 2–16 g Bolker, B. and Pacala, S. (1999) Spatial moment equations for plant competition: understanding spatial strategies and the advantages of short dispersal. Am. Nat. 153, 575–602 whether invasion is promoted or inhibited by harshness [24]. An invader will be at an advantage if its maintenance requirement does not increase as much as that of a resident with environmental harshness, or if it has a stronger response to increased resources than the residents (Box 2). Environmental fluctuations in time and space also have major effects. The key issues again are differential effects of the fluctuations on invaders and residents, with the added parameter that different species might be favored at different times and in different places [4,5,25] (Box 3). Environment–resource interactions naturally have parallels in environment–natural enemy interactions, but one should also consider natural enemy–resource interactions. Indeed, important http://tree.trends.com 173 invader advantage might accrue as a result of these interactions, because residents and invaders could be differentially susceptible to specialist natural enemies of the residents. In particular, high densities of specialist natural enemies should lead to lower densities of resident species, increasing resource availability [24,30,36]. Although generalist natural enemies might have similar effects on resources as the specialists, the increased resource availability for an invader could be countered by a decrease in escape opportunity [24,30]. The net outcome of all these different interactions determines the magnitude and nature of the niche opportunities provided by the community. How niche opportunities arise Natural enemy escape opportunities Most communities provide escape opportunities because they do not have the specialist natural enemies of invaders from geographically distant locations [7]. Although invasions are sometimes compared with range expansions [5,37], escape opportunities imply an important distinction, because specialist natural enemies must be lost at much lower rates during range expansions than they are during invasions of relatively small numbers from great distances. Invaders that offset losses to natural enemies in their native range by having high fecundity or individual growth (grazed plants and clonal animals) [38] could gain a strong advantage in a system without their specialist natural enemies. Potentially diminishing this advantage are generalist naturalist enemies to which the invader might be particularly vulnerable in the invaded location because it has no evolutionary history with them and might not be adequately protected against them [34]. The spectacular success of biological control for some invaders, however, implies that loss of natural enemies is sometimes an important escape opportunity [7,39]. Escape opportunities can allow a species to win in resource competition in a similar way to a low maintenance requirement (Box 2), potentially allowing an invader to reach high densities and have a large effect on resources. Apparent competition can have a similar outcome. An invader with few specialist natural enemies could rise to a high density, maintaining generalist natural enemies that severely impact the native community. Resource opportunities Disturbance is commonly assumed to release resources and provide opportunities for invaders [5], an idea that has been generalized to consider any form of temporal variation in resource availability [4,5]. As emphasized by spatio-temporal resource competition theory (Box 3) an invader still must have some advantage over residents. However, that advantage might occur at particular times or in Opinion TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 Number of exotic species 174 Number of native species TRENDS in Ecology & Evolution Fig. 1. Reconciliation of relationships between invasion success and species richness on different spatial scales. In this illustration, extrinsic conditions are assumed to be the same within each cluster of points but to differ between clusters. Within any cluster, higher numbers of native species lead to poorer niche opportunities for invaders, generating the negative relationship between the numbers of alien species and native species often observed in models, experiments and at small spatial scales. However, extrinsic factors can vary considerably on broad spatial scales. If extrinsic factors that favor high numbers of native species also directly increase niche opportunity for invaders, changes in these extrinsic factors will lead to clusters of points whose mean numbers of alien and native species are positively related, as depicted. Thus, there is an overall positive relationship between alien and native species when the data are combined on a broad spatial scale. climate, and North America in comparison with Eurasia [29]. Greater disruption by humans and greater rates of commerce between geographically similar regions might contribute to some of these elevated rates, but particular features of the communities themselves could also contribute [45]. Species in different systems might vary in competitive ability [11,26] or their degree of specialization [29] – that is, the breadth of conditions under which individual members have positive responses to their environment. In the presence of tradeoffs that benefit specialization [46], several specialized species would reduce resources more effectively than one generalist species covering the same range of circumstances. The maturity concept (Box 1) might explain such community differences: communities that have had less time to assemble, and less time for their constituent species to adapt to the local conditions, are likely to have fewer species with broader niches. Their species might also have lower competitive abilities than those in communities that have had a longer time under their present environmental regime. These communities tend to be less invasion resistant (Box 1). Similar effects on invasion resistance might result from the size of the species pool from which a community has assembled. Maturity undoubtedly also affects invasion resistance through escape opportunities, but clear predictions in this area are not so apparent. Variation in niche opportunities with resident diversity particular places, or it might be in a life-history trait, such as colonizing ability (Box 3). Sher and Hyatt [4] emphasize that an advantage to invaders commonly arises through disruption of the historical pattern of resource supply and consumption. There are many ways in which human activities disrupt historical patterns of resource fluctuations, including alteration of patterns of fire [40], harvesting of biomass, nutrient enrichment [12], alteration of patterns of spatial heterogeneity, and climate change [1,41,42]. Resident species might not be adapted to the changed environmental conditions, lessening their ability to reduce resource availability uniformly in time and space, and thus providing resource opportunities for invaders. Some invaders, such as species that inhabit human disturbed environments in their native range, might have critical adaptations to human disturbed environments that resident species lack [43,44], giving them the advantages they need for successful invasion. Community maturity Do natural communities vary in the niche opportunities that they provide, independently of the disruptions discussed above? Particular systems and geographical regions have relatively high rates of invasions. Among these are freshwater systems, oceanic islands, regions with a Mediterranean http://tree.trends.com Maturity is one theoretical approach to explaining invasion resistance. Ideally, invasion resistance could be predicted from directly observable community properties. In a classic work, Elton [47] proposed that communities with high species diversity should be invasion resistant. Indeed, models and some experimental studies suggest that high species diversity does lead to invasion resistance – that is, there is a negative relationship between invasion success and species diversity [48–51]. However, largescale observational patterns mostly show that more diverse systems tend to have higher numbers of exotic species [3,51,52]. There have been various attempts to understand these conflicting patterns. Scale and the role of covarying factors Species diversity varies widely with physical extrinsic factors, such as latitude, climate (given latitude), soils and the supply rates of physical resources to a system. This observation can help explain the discrepancy between different studies. If extrinsic factors favorable to high species diversity also lower invasion resistance, the positive relationship between species diversity and invasion success seen on broad spatial scales is explained [50]. A negative pattern of invasion success as a function of diversity, for fixed extrinsic conditions, is consistent with this proposal, as illustrated in Fig. 1: Opinion TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 Box 4. Future directions The niche opportunity framework raises many questions and provides many avenues for new research. The following are some of the most immediate. • Interactions between resource and escape opportunity: much of the recent invasion literature emphasizes resources. However, an invader released from natural enemies would have a low maintenance requirement and therefore a low R * value. It would thus be a strong competitor. Hence, the cause of the invasion might appear to be a resource opportunity when, in fact, it is an escape opportunity. Studies of the interaction between natural enemies and competition in the native range of the invader, and in the invaded community, would resolve this issue. • Community maturity: the theoretical concept of community maturity has been explored implicitly through models of community assembly [a]. However, there is a need for systematic studies of invasion resistance distinguishing the effects of time, species pool, the number of established species and established functional diversity. Important challenges are to understand the accumulations of natural enemies over time, their degree of specialization and their interactions with resources. • Covarying extrinsic factors in field studies: covarying extrinsic factors easily confound the relationship between invasion resistance and diversity. There is a need for field techniques to control for extrinsic factors. Methods of data analysis accounting for covarying extrinsic factors also need to be developed. • Improved understanding of coexistence mechanisms in nature: a better understanding of how species coexist in natural systems would give a better appreciation of the kinds of niche opportunity that a system might provide. For example, studies of changes in dominance patterns over time and in space could test whether species coexist by having different responses to spatially and temporally varying environmental factors. This information would also reveal the kinds of changes to the system that might favor invasion. Reference a Morton, R.D. and Law, R. (1997) Regional species pools and the assembly of local ecological communities. J. Theor. Biol. 187, 321–331 Acknowledgements K.S. is a collaborator via a fellowship under the OECD Co-operative Research Programme: Biological Resource Management for Sustainable Agricultural Systems and also acknowledges the Australian CRC for Weed Management Systems, NMFS (grant to M. Mangel, UC Santa Cruz) and NIH/NSF Ecology of Infectious Diseases grant (1R01ES11067-01) for support. P.C. was supported by NSF grant DEB 9981926. We also thank Ottar Bjørnstad, Ryan Keane, Mark Lonsdale, Marc Mangel, Peter Moyle, Bill Murdoch, Marcel Rejmánek, Jay Stachowicz, Don Strong, Mark Torchin, Michael Turelli and Mark Williamson for comments. the broad-scale positive relationship is the outcome of combining data from a series of negative relationships, where each negative relationship comes from different extrinsic conditions. This reconciliation of conflicting patterns is consistent with the outcome of models [51] in which extrinsic factors are not generally varied. Species diversities differ because of different sizes of the species pool colonizing the local system, or different amounts of time for species to accumulate in the local system, or simply due to chance: randomness in the process of community assembly leaves some systems with fewer species than others. In all these ways of varying species diversity, there is a consistent tendency in models for invasion success to decrease with species diversity. Generally, equivalent results have been obtained by experimental studies that carefully control extrinsic factors, or randomize them, and define species diversity as the number of species supplied to the system [53]. By contrast, studies that define species diversity as the number of species successfully established might confound uncontrolled variation in extrinsic factors, including propagule pressure. According to Fig. 1, a positive relationship between invasion success and diversity could result. The role of positive interactions An alternative explanation of positive relationships between species diversity and invasion success, which has some support from experiments in agricultural systems, is that high species diversity creates niche opportunities – for example, by mutualisms, both http://tree.trends.com 175 direct and indirect, that facilitate the entry of other species [54]. The modeling and experimental studies that found negative relationships might not have provided the conditions for sufficiently beneficial mutualisms to occur, possibly explaining why invasion success did not increase with diversity. The role of niche differentiation Theoretical explanations of why higher species diversity might confer invasion resistance, when extrinsic factors are controlled, depend on how the niches of the various residents and invaders relate to one another. According to the empty niche hypothesis [55], lower species diversity might simply mean the existence of circumstances where resources are not being exploited efficiently because species with suitable niches are lacking. Niche opportunities therefore exist for species able to benefit from resources in those particular circumstances [7]. In this case, it should not be just the diversity of resident species that matters but how their niches differ functionally [56], including their spatial and temporal patterns of effects on resources [48]. At the opposite extreme is the sampling hypothesis, where species are not differentiated functionally but vary in their ability to reduce resources [57], or (presumably) to maintain natural enemies. According to this hypothesis, higher diversity does not broaden the circumstances under which resources are exploited efficiently but instead increases the probability that a high-ranking competitor is present. Invasion success depends not on filling a vacant niche but on being a better exploiter of resources or a better avoider of natural enemies than resident species. However, a competitor’s rank might vary in space and time, allowing a high diversity of species to be maintained in the system [25] (Box 3). Thus, invader success depends on finding a time or place where it is superior to resident species, and the distinction between the empty niche hypothesis and the sampling hypothesis is lost [57,58]. Conclusion Over much of its history, invasion ecology has developed on a relatively separate path from other areas of ecology, potentially to the detriment of the discipline [59]. The framework presented here, however, shows how core issues of invasion ecology can be discussed as topics in community ecology. Recent advances in community ecology theory have made this possible by providing detailed predictions about topics of particular importance in invasion ecology, such as resource and natural enemy interactions [30,32], and disturbance and more general kinds of variation in space and time [24,25,60]. The link between community and invasion ecology is a natural one, because the essential criterion for a species to persist in a community is its ability to increase from low density, 176 Opinion TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 which is also the condition for an alien to be able to invade a community. This means that invasion ecology has the potential to contribute greatly to community ecology. Invasions provide case studies on particular communities subject to perturbation by References 1 Vitousek, P.M. et al. (1997) Introduced species: a significant component of humancaused global change. New Zealand J. Ecol. 21, 1–16 2 Kolar, C.S. and Lodge, D.M. (2001) Progress in invasion biology: predicting invaders. Trends Ecol. Evol. 16, 199–204 3 Lonsdale, W.M. (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80, 1522–1536 4 Sher, A.A. and Hyatt, L.A. (1999) The disturbed resource-flux invasion matrix: a new framework for patterns of plant invasion. Biol. Inv. 1, 107–114 5 Davis, M.A. et al. (2000) Fluctuating resources in plant communities: a general theory of invasibility. J. Ecol. 88, 528–534 6 Keane, R.M. and Crawley, M.J. (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17, 164–170 7 Mack, R. et al. (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10, 689–710 8 Williamson, M. (1996) Biological Invasions, Chapman & Hall 9 Veltman, C.J. et al. (1996) Correlates of introduction success in exotic New Zealand birds. Am. Nat. 147, 542–557 10 Shigesada, N. and Kawasaki, K. (1997) Biological Invasions: Theory and Practice, Oxford University Press 11 Petren, K. and Case, T. (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77, 118–132 12 Jefferies, R.L. (2000) Allochthonous inputs: integrating population changes and food web dynamics. Trends Ecol. Evol. 15, 19–22 13 Settle, W.H. and Wilson, L.T. (1990) Invasion by the variegated leafhopper and biotic interactions: parasitism, competition and apparent competition. Ecology 71, 1461–1470 14 Torchin, M.E. et al. (1996) Infestation of an introduced host, the European green crab, Carcinus maenas, by a symbiotic nemertean egg predator, Carcinonemertes epalti. J. Parasitol. 82, 449–453 15 Moyle, P.B. and Light, T. (1996) Fish invasions in California: Do Abiotic Factors Determine Success? Ecology 77, 1666–1670 16 Sutherst, R.W. et al. (1999) CLIMEX: Predicting the Effects of Climate on Plants and Animals, CSIRO Publishing 17 Tilman, D. (1982) Resource Competition and Community Structure, Princeton University Press 18 Davis, M.A. et al. (1998) Competition between tree seedlings and herbaceous vegetation: support for a theory of resource supply and demand. J. Ecol. 86, 652–661 19 Murdoch, W.W. et al. (1996) Competitive displacement and biological control in parasitoids: A model. Am. Nat. 148, 807–826 20 Byers, J.E. (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81, 1225–1239 http://tree.trends.com invaders; they also provide the challenge of explaining invader success and invader impact. Indeed, there is every reason to expect a healthy synergy between invasion ecology and community ecology (Box 4). 21 Holway, D.A. and Suarez, A.V. (1999) Animal behavior: an essential component of invasion biology. Trends Ecol. Evol. 14, 328–330 22 Thompson, J.D. (1991) The biology of an invasive plant. BioScience 41, 393–401 23 Leibold, M.A. (1998) Similarity and local coexistence of species from regional biotas. Evol. Ecol. 12, 95–110 24 Chesson, P. and Huntly, N. (1997) The roles of harsh and fluctuating conditions in the dynamics of ecological communities. Am. Nat. 150, 519–553 25 Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 26 Callaway, R.M. and Aschehout, E.T. (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290, 521–523 27 Mack, M.C. and D’Antonio, C.M. (1998) Impacts of biological invasions on disturbance regimes. Trends Ecol. Evol. 13, 195–198 28 Simberloff, D. and VonHolle, B. (1999) Positive interactions of nonindigenous species. Biol. Inv. 1, 21–32 29 Huston, M. (1994) Biological Diversity, Cambridge University Press 30 Holt, R.D. et al. (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am. Nat. 144, 741–771 31 Holt, R.D. and Lawton, J.H. (1994) The ecological consequences of shared natural enemies. Annu. Rev. Ecol. Syst. 25, 495–520 32 Grover, J.P. and Holt, R.D. (1998) Disentangling resource and apparent competition: realistic models for plant–herbivore communities. J. Theor. Biol. 191, 353–376 33 Murdoch, W.W. et al. (1985) Biological control in theory and practice. Am. Nat. 125, 344–366 34 Mack, R.N. (1996) Biotic barriers to plant naturalization. In Proceedings of the IX International Symposium on Biological Control of Weeds (Moran, V.C. and Hoffman, J.H., eds), pp. 39–46, University of Cape Town 35 Larcher, W. (1983) Physiological Plant Ecology, Springer-Verlag 36 Grover, J.P. (1994) Assembly rules for communities of nutrient-limited plants and specialist herbivores. Am. Nat. 143, 258–282 37 Thompson, K. et al. (1995) Native and alien invasive plants: more of the same? Ecography 18, 390–402 38 Mauricio, R. et al. (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78, 1301–1311 39 Hawkins, B.A. and Cornell, H.V., ed. (1999) Theoretical Approaches to Biological Control, Cambridge University Press 40 D’Antonio, C.M. (2000) Fire, plant invasions and global changes. In Invasive Species in a Changing World (Mooney, H.A. and Hobbs, R.J., eds), pp. 65–93, Island Press 41 Dukes, J.S. and Mooney, H.A. (1999) Does global change increase the success of biological invaders? Trends Ecol. Evol. 14, 135–139 42 Mooney, H.A. and Hobbs, R.J., ed. (2000) Invasive Species in a Changing World, Island Press 43 Brown, J.H. (1989) Patterns, modes and extents of invasions by vertebrates. In Biological Invasions: A Global Perspective (Drake, J.A. and Mooney, H.A., eds), pp. 85–110, John Wiley & Sons 44 Drake, J.A. and Mooney, H.A., eds (1989) Biological Invasions: A Global Perspective, John Wiley & Sons 45 Niemelä, P. and Mattson, W.J. (1996) Invasion of North American forests by European phytophagous insects. BioScience 46, 741–753 46 Rosenzweig, M.L. (1995) Species Diversity in Space and Time, Cambridge University Press 47 Elton, C. (1958) The Ecology of Invasions by Animals and Plants, Methuen 48 Stachowicz, J.J. et al. (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286, 1577–1579 49 Knops, J.M.H. et al. (1999) Effects of plant species richness on invasions dynamics, disease outbreaks, insect abundances, and diversity. Ecol. Lett. 2, 286–293 50 Naeem, S. et al. (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91, 97–108 51 Levine, J.M. and D’Antonio, C.M. (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87, 15–26 52 Stohlgren, T.J. et al. (1999) Exotic plant species invade hot spots of native plant diversity. Ecol. Monogr. 69, 25–46 53 Levine, J.M. (2000) Species diversity and biological invasions: relating local process to community pattern. Science 288, 852–854 54 Palmer, M.W. and Maurer, T.A. (1997) Does diversity beget diversity? A case study of crops and weeds. J. Veg. Sci. 8, 235–240 55 Simberloff, D. (1995) Why do introduced species appear to devastate islands more than mainland areas? Pac. Sci. 49, 87–97 56 Dukes, J.S. (2001) Biodiversity and invasibility in grassland microcosms. Oecologia 126, 563–568 57 Crawley, M.J. et al. (1999) Invasion resistance in experimental grassland communities: species richness or species identity? Ecol. Lett. 2, 140–148 58 Chesson, P. et al. (2001) Environmental niches and ecosystem functioning. In Functional Consequences of Biodiversity (Kinzig, A. et al., eds), pp. 213–245, Princeton University Press 59 Davis, M.A. et al. (2001) Charles S. Elton and the dissociation of invasion ecology from the rest of ecology. Div. Distrib. 7, 97–102 60 Bolker, B. and Pacala, S. (1999) Spatial moment equations for plant competition: understanding spatial strategies and the advantages of short dispersal. Am. Nat. 153, 575–602 454 Review TRENDS in Ecology & Evolution Vol.16 No.8 August 2001 Viewing invasive species removal in a whole-ecosystem context Erika S. Zavaleta, Richard J. Hobbs and Harold A. Mooney Eradications of invasive species often have striking positive effects on native biota. However, recent research has shown that species removal in isolation can also result in unexpected changes to other ecosystem components. These secondary effects will become more likely as numbers of interacting invaders increase in ecosystems, and as exotics in late stages of invasion eliminate native species and replace their functional roles. Food web and functional role frameworks can be used to identify ecological conditions that forecast the potential for unwanted secondary impacts. Integration of eradication into a holistic process of assessment and restoration will help safeguard against accidental, adverse effects on native ecosystems. Erika Zavaleta* Harold A. Mooney Dept of Biological Sciences, Stanford University, Stanford, CA 94305, USA. *e-mail: [email protected] Richard J. Hobbs School of Environmental Science, Murdoch University, Murdoch, WA 6150, Australia. Invasive alien species interact with other elements of global change to cause considerable damage to managed and natural systems and to incur huge costs to society1. In response, several measures have been developed and deployed to control, contain or eradicate a wide range of invasive species in affected areas. Where possible, ERADICATION (see Glossary) is the favored approach. Control, which reduces the presence of the invader, and containment, which limits further spread, both require indefinite investments of time, tools and money to keep an invader at bay. Although eradication can require large short-term investments, successful removal can be achieved within months or years and gives the best chance for native biodiversity to recover. The results of eradication efforts so far are encouraging and have been detailed recently2. Many case studies demonstrate success for a range of taxa, particularly on small islands and at local scales. Additional examples include the removal of the exotic little red fire ant Wasmannia auropunctata from Santa Fe Island in the Galapagos3 (which resulted in the increase in density of several native ant species), and the nearly complete removal from Laysan Island, Hawaii of the exotic annual grass Cenchrus echinatus, which once covered 30% of the vegetated area of the island (E.N. Flint, unpublished). Successful eradications often lead to dramatic recovery of native species and ecosystems. Removal of introduced rabbits from Pacific islands off Mexico (C.J. Donlan, unpublished) and the USA have allowed recovery of two rapidly declining endemic species of native succulents Dudleya linearis and D. traskiae4. Lowland vegetation on Santa Fe Island has recovered steadily following the removal of exotic goats Capra hircus nearly 30 years ago. However, other cases suggest that more refined and integrated approaches to invasive removal could improve results. Successes are still largely confined to small islands. The ecological context of eradication is http://tree.trends.com increasingly complex. Major damage caused by longestablished invaders, systems that are affected by multiple invaders, and systems that are affected by both invaders and other global changes are now common. In these settings, straightforward deployment of standard eradication tools, such as poisons, trapping and mechanical harvesting, might not accomplish the desired level of recovery of native ecosystems5. We suggest that, although there is a crucial need for the continued development and application of effective eradication methodologies, a parallel need exists to place these methodologies in the context of the overall ecosystem that is being managed. Ideally, there should be both: (1) pre-eradication assessment, to tailor removal to avoid unwanted ecological effects; and (2) post-removal assessment of eradication effects, on both the target organism and the invaded ecosystem. The requirements for successful removal of an invader have been discussed recently2. We focus on the possible impacts that result from the successful removal of invasive species, regardless of the methods employed to remove them. We reviewed recent literature for examples where the successful eradication of invasives had or was likely to have important secondary impacts, a task that was made difficult by the relatively few verified eradication successes that included the monitoring of postremoval system behavior. Eradication: what can go wrong Successful eradication efforts have generally benefited biological diversity. However, there is also evidence that, without sufficient planning, successful eradications can have unwanted and unexpected impacts on native species and ecosystems. These inadvertent impacts are of many types. Excessive poisoning of non-target organisms and transfer of poisons up food chains6 are problems that can result from the removal method used7,8. Some eradication efforts fail because they do not eliminate the target organism, because they either miss individuals or do not include steps to reduce post-eradication susceptibility to reinvasion3. Eradication alone might not allow ecosystems to recover, because some invaders change the condition of the habitat so as to render it unsuitable for native species. For instance, in sites from the Middle East to the western USA, high soil salinity is caused by the invasive ice plant Mesembryanthemum crystallinum, and tamarisk Tamarix spp., which makes it difficult for salt-sensitive native species to re-establish9. In these cases, eradication must be followed by additional site restoration. 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02194-2 Review TRENDS in Ecology & Evolution Vol.16 No.8 August 2001 Box 1. When a harmful exotic harbors an endangered native species Exotic saltcedar Tamarix spp. shrubs have replaced much of the native riparian vegetation of the arid western USA, where they consume large quantities of water, narrow river channels, salinize soil and degrade wildlife habitata. Saltcedar removal has been repeatedly delayed in parts of its range because it provides significant nesting habitat for an endangered native songbirdb. The southwestern willow flycatcher Empidonax trailii extimus, currently reduced to fewer than 500 breeding pairs, nested historically in riparian cottonwood (Populus spp.)–willow (Salix spp.) stands in the southwestern USA (Refs c,d). Urbanization, agriculture, fire, water diversion and livestock grazing all contributed to the decline of its native habitatb. The replacement of much of the habitat that remained by saltcedar required the flycatcher to make use of the invader, which it seems to prefer in some areas, despite its reduced breeding successe,f. Stepwise saltcedar removal could strongly benefit the flycatcher by giving native trees the opportunity to re-establish and provide replacement habitatg. However, some saltcedar-invaded areas might no longer be able to support native vegetation, because lowered water tables and saline soils, the results of saltcedar dominance, might complicate native re-establishmenth–j. Region-wide flood suppression hinders re-establishment of flood-associated native species such as cottonwoods and increases the likelihood of saltcedar reinvasionj,k. Managers are confident that, if accompanied by planning and careful restoration, saltcedar removal can benefit the endangered flycatcher as well as other native speciesg. However, poorly planned removal without steps such as flooding and vegetation restoration, might fail, harming an endangered species in the process. References a Zavaleta, E.S. (2000) Valuing ecosystem services lost to Tamarix invasion in the United States. In Invasive Species in a Changing World (Mooney, H.A. and Hobbs, R.J., eds), pp. 261–300, Island Press b USFWS (1997) Endangered and threatened wildlife and plants; final determination of critical habitat for the southwestern willow flycatcher. Fed. Reg. 62, 39129–39147 c Rosenberg, K.V. et al. (1991) Birds of the Lower Colorado River Valley, University of Arizona Press d Sogge, M.K. et al. (1997) A Southwestern Willow Flycatcher Natural History Summary and Survey Protocol, National Park Service e DeLoach, C.J. et al. (1999) In Ecological Interactions in the Biological Control of Saltcedar (Tamarix sp.) in the US: Toward a New Understanding, US Department of Agriculture f McKernan, R.L. and Braden, G. (1999) Status, Distribution, and Habitat Affinities of the Southwestern Willow Flycatcher Along the Colorado River; Year 3 – 1998, US Dept of the Interior–Bureau of Reclamation g Dudley, T.L. et al. (2001) Saltcedar Invasion of Western Riparian Areas: Impacts and New Prospects for Control, US Department of Agriculture h Jackson, J. et al. (1990) Assessment of the Salinity Tolerance of Eight Sonoran Desert Riparian Trees and Shrubs, US Dept of the Interior–Bureau of Reclamation i Shafroth, P.B. et al. (1995) Effects of salinity on establishment of Populus fremontii (cottonwood) and Tamarix ramosissima (saltcedar) in southwestern United States. Great Basin Nat. 55, 58–65 j Taylor, J.P. and McDaniel, K.C. (1998) Restoration of saltcedar infested flood plains on the Bosque del Apache National Wildlife Refuge. Weed Technol. 12, 345–352 k Stromberg, J. (1998) Dynamics of Fremont cottonwood (Populus fremontii) and saltcedar (Tamarix chinensis) population along the San Pedro River, Arizona. J. Arid Environ. 40, 133–155 455 increases in exotic plant populations. Removal of one invader can lead to increased impacts of another invader; for example, when removal of exotic prey leads to increased predation on native prey by exotic predators10. Finally, removal of invasive plant species can reduce habitat or resources available for native fauna if the removal is not accompanied by further restoration measures (Box 1). These unexpected outcomes will become more probable both as the variety of interacting invaders contained in an ecosystem increases, and as exotics in late stages of invasion largely or wholly eliminate native species and replace their functional roles. Although researchers have begun to explore the implications of multiple, interacting invaders, little attention has been paid to the implications of these interactions for eradication efforts. Secondary effects: a conceptual framework A useful basis from which to tackle when and why secondary effects of eradication occur is that systems containing invasives function according to the same basic principles as do other systems. Invaded systems can, therefore, be considered using the frameworks that are usually used to analyze community and ecosystem dynamics. Trophic cascades in multiply invaded systems A large literature has been devoted to how food-web interactions limit populations of producers, consumers and predators11–13. Much work has been done on the relative roles of top-down regulation of food-web components by higher-level consumers or predators, and of bottom-up regulation of populations by food availability or resource limitation. Evidence from several ecosystem types shows that both top-down and bottom-up population regulation of producers and consumers occur under some conditions14–16. The existence of these regulatory links can give rise to TROPHIC CASCADES16,17 (but see Ref. 13). When combined with the use of simple terrestrial food webs6 (Fig. 1), this framework helps to explain how many animal eradications have allowed population recovery of native species. Removal of an exotic predator can release native prey from strong top-down regulation, increasing prey abundance with potential cascading impacts on other food-web components, including native predators (Fig. 1b). Similarly, exotic herbivores in the absence of predators can become sufficiently abundant to exert top-down pressure on native plants14. Removal of these herbivores can lead to rapid recovery of native plant populations4. Predator–prey interactions Successful eradications can also have undesired effects that result from the successful removal of the invader. In several cases, removal of one exotic species has led to the establishment or increase of one or more other invasive species. For example, several eradications of exotic herbivores have been linked to http://tree.trends.com However, the presence of multiple invaders at different trophic levels complicates matters. Consider the case where an exotic predator and an exotic prey species co-occur (Fig. 1c). Removal of the invasive predator only could lead to MESOPREDATOR RELEASE (release of the invasive prey from top-down Review 456 Fig. 1. Idealized food webs indicating trophic interactions between species. Closed boxes represent exotic species and open boxes represent native species. Arrow thickness indicates the strength of trophic interaction. Font size represents population size. (a) shows a community containing a single exotic predator. In (b), removal of this predator increases native prey populations. (c) shows a community containing both an exotic predator and an exotic herbivore. In (d), removal of only the exotic predator releases the exotic herbivore population, with cascading impacts on two plant species. (e) shows a community containing both an exotic herbivore and an exotic plant species. In (f), removal of the exotic herbivore only releases the exotic plant population. TRENDS in Ecology & Evolution Vol.16 No.8 August 2001 (c) (a) Predator 1 Consumer 2 Consumer 1 Plant 1 Predator 2 Plant 2 (e) Predator 1 Predator 3 Consumer 3 Plant 3 Plant 4 (b) Consumer 1 Plant 1 Predator 2 Consumer 2 Plant 2 Consumer 2 Consumer 1 Plant 1 Predator 2 Plant 2 Predator 3 Plant 3 Consumer 3 Plant 3 Plant 4 Consumer 2 Consumer 1 Plant 4 Plant 1 Predator 2 Plant 2 Predator 3 Consumer 3 Plant 3 Plant 4 (f) Predator 1 Predator 2 Predator 3 Consumer 1 Consumer 2 Consumer 3 Plant 1 Plant 2 Plant 3 Plant 4 Predator 1 Consumer 1 Plant 1 Predator 2 Consumer 2 Plant 2 Predator 3 Consumer 3 Plant 3 Plant 4 TRENDS in Ecology & Evolution regulation) (Fig. 1d). If the exotic prey consume native species, the removal of the exotic top predator could lead to net negative impacts on native populations of conservation value18. For example, exotic cats on Stewart Island, New Zealand, prey upon the kakapo Strigops habroptilus, an endangered flightless parrot. However, the diet of the cats consists overwhelmingly of the three species of exotic rats on the island19. Cat eradication would probably increase the impact of rats on the kakapo as well as on other native biota unless rats were simultaneously removed. The potential for mesopredator release following cat eradication is widespread. Introduced rats Rattus spp., house mice Mus musculus, and/or rabbits Oryctolagus cuniculus co-occur with exotic cats on 22 islands where the diets of cats have been studied. In nearly every case, cats exert important top-down controls on these other exotics by preying heavily on rabbits if they are present, and heavily on rats if rabbits are not present20 (Table 1). Mice are also an important part of the diet of feral cat on islands at temperate, but not tropical, latitudes20. The potential for these trophic effects is probably strongest on islands lacking native predators; however, it applies, in principle, to any system in which exotic predator populations take advantage of abundant exotic prey. The effects of mesopredator release can cascade to alter ecosystem-scale properties as well as altering native populations. Studies before cat eradication on subantarctic Marion Island showed that the cats ate Table 1. Importance of exotic rats in the diet of introduced cats on islandsa Islands without introduced rabbits Occurrence of rats in diet (%) Islands with introduced rabbitsb Occurrence of rats in diet (%) Galapagos: Isabela Santa Cruz Lord Howe Raoul Little Barrier Stewart Campbell 73 88 87 86 39 93 95 Gran Canaria Te Wharau, NZ Kourarau, NZ Orongorongo, NZ Mackenzie, NZ Kerguelen Macquarie 4 3 Trace 50 2 0 3 aData Consumer 3 (d) Predator 1 Predator 1 Predator 3 from Ref. 20. NZ, New Zealand. bAbbreviation: http://tree.trends.com many exotic house mice, which prey heavily upon a flightless endemic moth Pringleophaga marioni, which is important to nutrient cycling21–23. Removal of the cats only might have allowed increases in mouse populations, causing cascading declines in endemic moth abundance and, ultimately, changes in soil nutrient availability. When exotic predators and prey co-occur, eradication of only the exotic prey can also cause problems by forcing the predator to switch to native prey. In New Zealand, introduced rats R. rattus and possums Trichosurus vulpecular are an important part of the diet of the stoat Mustela ermina, an exotic mustelid10. Efforts to remove all three species by poisoning the prey species had an unexpected result: the stoat populations were not eliminated by either the prey eradication or the poison application and, in the absence of abundant exotic prey, the stoats switched their diets to native birds and bird eggs. Without prey eradication, the co-occurrence of exotic predators and exotic prey can impact heavily on native prey populations by HYPERPREDATION. The availability of abundant exotic prey can inflate exotic predator populations, which then increase their consumption of indigenous species24. This phenomenon was first elaborated to explain why native Australian mammals suffered population declines in areas invaded by cats only if exotic rabbit and mouse densities were also high25. The removal of exotic prey to curb hyperpredation of native species by exotic predators has been suggested26. However, managers must consider carefully whether native populations can withstand further, temporary increases in predation when the inflated predator population no longer has exotic prey to sustain it. Herbivore–plant interactions When exotic herbivores and plants co-occur (Fig. 1d), control or eradication of only the exotic plants could, in theory, lead to increased exotic herbivory on native plants. However, we do not know of a case in which this has occurred. This might reflect the paucity of successful plant eradications, the prioritization of Review TRENDS in Ecology & Evolution Vol.16 No.8 August 2001 animal removals from multiply invaded ecosystems, or an absence of strict bottom-up regulation of exotic herbivores by plant biomass availability. When exotic herbivores and plants co-occur, eradication of the herbivores only can lead to release of exotic plants from top-down control (Fig. 1f). In nearly all documented cases where exotic plants co-occur with exotic herbivores on islands, herbivore removal has had mixed results for native vegetation (but see Refs 27,28). Feral herbivore removal from Santa Catalina Island, Channel Island National Park, led to an increase in native species richness, but also to large absolute and relative increases in cover by exotic annuals29. Rabbit eradication on Round Island, Mauritius, led to strong recovery of three endemic or locally restricted tree species (Latania loddigesii, Pandanus vandermeerschii and Hyophorbe lagenicaulis) and six reptile species [two skinks (Leiolopisma telfaririi and Scelotes bojerii), three geckos (Phelsuma guentheri, P. ornata and Nactus serpensinsula) and a snake (Casarea dussumerii)], including five endemics30. However, rabbit removal also caused the spectacular release of a previously sparse exotic grass Chloris barbata, rendering it a significant component of the vegetation on the island30 (Box 2). Asiatic water buffalo Bubalus bubalis eradication from Kakadu National Park, Australia spurred large-scale regeneration of the wetlands of the park31. However, alien plant species also proliferated, in particular, introduced para grass Brachiaria mutica, which now covers approximately 10% of the major floodplain habitats in the park. Although the removal of feral pigs Sus scrofa, sheep Ovis aries and goats has allowed some native plant species to recover slightly in Hawai’i32, many Hawai’ian lowland grasslands have responded to ungulate removal with increases in the cover of flammable exotic grasses33. Accompanying increases in fire frequency accelerate a positive feedback loop among invasive grass establishment, fire, and loss of native woodlands and forest34. The effects of exotic herbivore removal on native vegetation, under certain circumstances, might also have indirect negative effects, because of the presence of other exotic animals. Rabbit removal on Macquarie Island in the Southern Ocean led to major increases in cover by a native tussock grass Poa foliosa, which is the preferred habitat of the introduced ship rat. Tussock expansion could bring the rats into contact with burrow-nesting bird colonies on the island, which have escaped rat predation so far35. Herbivore removal from islands has strong negative effects on vegetation in some cases. The removal of sheep and cattle Bos taurus from Santa Cruz Island led to an explosive expansion of exotic fennel Foeniculum vulgare, starthistle Centaurea solstitialis, and other introduced herbs, increases in relative cover of exotics, but the observable recovery of only one native species, Bishop pine Pinus muricata, after nine years of monitoring36–38. Moreover, the sudden expansion of exotic forbs provided abundant food for feral European bee Apis mellifera, colonies, and complicated eventual bee eradication from the island39. The greatest potential for negative impacts on native vegetation perhaps exists when herbivore eradication removes the disturbance that is necessary to suppress establishment of late successional (tree or shrub) exotics40. The removal of feral cattle from degraded grasslands on San Cristobal Island in the Galapagos allowed previously suppressed exotic guava Psidium guajava to grow rapidly into dense, extensive thickets41. Box 2. Replacing extinct herbivores in the Mascarene Islands Before their extinction, two species of giant tortoise (Geocholone triserrata and G. inepta), endemic to the Mascarene Islands, browsed the native vegetation and dispersed fruits of endemic trees such as the Ile aux Aigrettes ebony Diospyros egrettarum. Trade in tortoise meat, together with the introduction of rats and pigs in the 16th–18th centuries, extirpated the native browsers from the archipelago. Introduced goats Capra hircus and rabbits Oryctolagus cuniculus replaced the tortoises as herbivores, suppressing numerous introduced grazing-intolerant plant species until the late 20th century. However, the eradication of exotic herbivores from Round Island and Ile aux Aigrettes in the 1970s and 1980s released populations of exotic weeds such as Chloris barbata on Round Island and false acacia Leucaena leucocephala on Ile aux http://tree.trends.com Aigrettes. Native tussock-forming grasses declined on Round Island, and increasingly tall exotic vegetation threatened lowgrowing endemics such as Aerva congesta, now found only on Round Island. To restore and maintain native vegetation, scientists at the Mauritian Wildlife Foundation are exploring the introduction of a taxonomic and functional I 457 substitute for the extinct tortoises, the Aldabran tortoise G. gigantia (Fig. I). Four adult Aldabran tortoises were released into a fenced enclosure on Ile aux Aigrettes in November 2000, and the first post-introduction vegetation survey took place in May 2001. Viable fruits of the endemic ebony have already been found dispersed in tortoise feces away from parent trees. It is hoped that the introduced tortoises will not only shift the competitive balance in favor of native plants, but also restore the broader functional roles of their extinct congeners in the ecosystems of the Mascarene archipelago. Reference a North, S.G. et al. (1994) Changes in the vegetation and reptile populations on Round Island, Mauritius, following eradication of rabbits. Biol. Conserv. 67, 21–28 458 Fig. 2. An adverse effect of eradication. The photographs show a camp site on Sarigan Island, Commonwealth of the Northern Mariana Islands, before (a) and after (b) successful eradication of feral goats Capra hircus and pigs Sus scrofa in 1998 explosively released a previously undetected exotic vine Operculina ventricosa. Arrows in (b) indicate the locations of the two buildings visible in (a). Reproduced, with permission, from Curt Kessler, Zoology Unlimited. Review TRENDS in Ecology & Evolution Vol.16 No.8 August 2001 for other biota. The case of Tamarix (Box 1) illustrates how, under certain conditions, consideration of this kind of undesirable impact can be important. (a) Conclusion (b) TRENDS in Ecology & Evolution In most settings, removing introduced herbivores is an important and reasonable first step in ecosystem restoration. However, in some cases (particularly on islands without native herbivores), herbivore removal might actually cause harm if there are no concurrent efforts to control exotic vegetation (Fig. 2). The clearest benefits from exotic herbivore removal are likely to occur in settings that are still dominated by native vegetation. In other settings, close monitoring after herbivore removal, as well as pre-eradication assessment, can help reduce unexpected negative consequences of the removal of invasives42. Native species dependence in exotic-dominated habitats Acknowledgements We thank Curt Kessler, Josh Donlan, John Mauremootoo, Robert Bensted-Smith, Bernie Tershy, Rick Van Dam, Dick Veitch, and Ingrid Parker and her lab group for their helpful input. Increasingly, exotic species have been present in ecosystems for long enough to dominate or replace native species and habitats. In these cases, an ecosystem or functional framework might be useful in which one asks whether removal of the invader will largely or entirely remove from the system a function necessary to other biota in it. For example, an invasive plant species might provide usable habitat for native fauna in the absence of original vegetation. Rapid removal of the invader without restoring native vegetation might not only increase the chances of a new invasion, but also leave native fauna without cover or food. Several examples of the potential for this type of problem have been described43. However, examples of successful eradications that actually led to such habitat loss have not been identified. This most probably reflects the lack of successful eradications of plants, which usually provide habitat http://tree.trends.com The type of species being removed, the degree to which it has replaced native taxa, and the presence of other non-native species can affect the eventual impacts of removal of an invasive species. Managers can take some simple steps to reduce surprise outcomes. Preassessment, including qualitative evaluation of: (1) trophic interactions among exotics and between natives and exotics; and (2) potential functional roles of exotics, is necessary for managers to anticipate the need for special planning. Post-eradication monitoring is also extremely valuable, not least because it allows managers to document the positive outcomes of eradication successes. It also provides the opportunity to learn from mistakes and gives managers the chance to curtail negative effects before they become severe. More frequent ecological studies that take advantage of eradication programss as being large-scale ecosystem experiments will speed the accumulation of knowledge about system responses to exotic species removals. Specific guidance for tailoring eradication efforts to complex situations is emerging. In the case of stoat–rat–opossum eradication in New Zealand10, follow-up study showed that the timing and method of poisoning used were important in determining stoat population declines (as a result of secondary poisoning) as well as determining effects on native birds44. A model of interactions between exotic cats and rabbits found that simultaneous removal of both species maximized the chances of success, but suggested that the next best alternative was to remove rabbits first and cats later26. Data from several cases show that attempts to restore a native species without removing all invaders that consume it are likely to fail45. Many attempts to reintroduce native marsupials to areas from which they have been extirpated have failed because of the presence of uncontrolled exotic terrestrial predators such as cats and foxes Vulpes fulva. Success rates of reintroductions are an order of magnitude greater (82% versus 8%) on islands without exotic predators46. As they accumulate, these kinds of analyses – whether based on post-eradication data or modeled on ecological principles – will enable the design of better eradication and restoration strategies. Invasive species eradication is an increasingly important component of the conservation and management of natural ecosystems. However, in natural systems, a shift in emphasis from strict invasives management towards broader ecosystem restoration goals is required. This will place more emphasis on the full diagnosis of causal factors and the desired ecological outcomes of eradications47. As knowledge about effective eradication methods accumulates, attention should turn to combining such methods with broader ecological principles to form cost-effective removal strategies that accomplish overall restoration goals. Review TRENDS in Ecology & Evolution Vol.16 No.8 August 2001 459 Glossary Eradication: removal of every individual and propagule of an invasive species so that only reintroduction could allow its return. Hyperpredation: abnormally high predation of indigenous prey species by a predator population that is inflated by the availability of highly abundant exotic prey. References 1 Mooney, H.A. and Hobbs, R.J., eds (2000) Invasive Species in a Changing World, Island Press 2 Myers, J.H. et al. (2000) Eradication revisited: dealing with exotic species. Trends Ecol. Evol. 15, 316–320 3 Abedrabbo, S. (1994) Control of the little fire ant, Wasmannia auropunctata, on Santa Fe Island in the Galapagos Islands. In Exotic Ants: Biology, Impact, and Control of Introduced Species (Williams, D.F., ed.), pp. 219–239, Westview Press 4 Clark, R. and Halvorson, W.L. (1987) The recovery of the Santa Barbara Island live-forever. Fremontia 14, 3–6 5 Donlan, C.J. et al. (2000) Island conservation action in northwest Mexico. In Proceedings of the Fifth California Islands Symposium (Browne, D.H. et al., eds), (CD-Rom), Santa Barbara Museum of Natural History 6 Innes, J. and Barker, G. (1999) Ecological consequences of toxin use for mammalian pest control in New Zealand: an overview. N. Z. J. Ecol. 23, 111–127 7 Cory, J.S. and Myers, J.H. (2000) Direct and indirect ecological effects of biological control. Trends Ecol. Evol. 15, 137–139 8 Simberloff, D. and Stiling, P. (1996) How risky is biological control? Ecology 77, 1965–1975 9 El-Ghareeb, R. (1991) Vegetation and soil changes induced by Mesembryanthemum crystallinum L. in a Mediterranean desert ecosystem. J. Arid Environ. 20, 321–330 10 Murphy, E. and Bradfield, P. (1992) Change in diet of stoats following poisoning of rats in a New Zealand forest. N. Z. J. Ecol. 16, 137–140 11 Hairston, N.G. et al. (1969) Community structure, population control, and competition. Am. Nat. 94, 421–425 12 Fretwell, S.D. (1987) Food chain dynamics: the central theory of ecology? Oikos 50, 291–301 13 Polis, G.A. and Strong, D.R. (1996) Food web complexity and community dynamics. Am. Nat. 147, 813–846 14 Terborgh, J. et al. (1999) The role of top carnivores in regulating terrestrial ecosystems. In Continental Conservation: Scientific Foundations of Regional Reserve Networks (Soule, M.E. and Terborgh, J., eds), pp. 39–64, Island Press 15 Polis, G.A. (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86, 3–15 16 Pace, M.L. et al. (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol. Evol. 14, 483–488 17 Polis, G.A. et al. (2000) When is a trophic cascade a trophic cascade? Trends Ecol. Evol. 15, 473–475 18 Courchamp, F. et al. (1999) Cats protecting birds: modelling the mesopredator release effect. J. Anim. Ecol. 68, 282–292 19 Karl, B.J. and Best, H.A. (1982) Feral cats on Stewart Island; their foods, and their effects on kakapo. N. Z. J. Zool. 9, 287–294 http://tree.trends.com Mesopredator release: rise in a population of one species caused by the removal of a species that preys upon it. It can lead to a net increase in predation on native populations of conservation concerna. Trophic cascade: when changes in one species affect the abundances of other species across more than one link in the food webb. 20 Fitzgerald, B.M. (1988) Diet of domestic cats and their impact on prey populations. In The Domestic Cat: The Biology of its Behavior (Turner, D.C., ed.), pp. 123–146, Cambridge University Press 21 Crafford, J.E. (1990) The role of feral house mice in ecosystem functioning on Marion Island. In Antarctic Ecosystems: Change and Conservation (Kerry, K.R. and Hempel, G., eds), pp. 359–364, Springer-Verlag 22 Bloomer, J.P. and Bester, M.N. (1990) Diet of a declining feral cat Felis catus population on Marion Island. S. Afr. J. Wildl. Res. 20, 1–4 23 Bloomer, J.P. and Bester, M.N. (1992) Control of feral cats on sub-Antarctic Marion Island, Indian Ocean. Biol. Conserv. 60, 211–219 24 Courchamp, F. et al. (2000) Rabbits killing birds: modelling the hyperpredation process. J. Anim. Ecol. 69, 154–164 25 Smith, A.P. and Quin, D.G. (1996) Patterns and causes of extinction and decline in Australian conilurine rodents. Biol. Conserv. 77, 243–267 26 Courchamp, F. et al. (1999) Control of rabbits to protect island birds from cat predation. Biol. Conserv. 89, 219–225 27 Van Vuren, D. and Coblentz, B.E. (1987) Some ecological effects of feral sheep on Santa Cruz Island, California, USA. Biol. Conserv. 41, 253–268 28 Coblentz, B.E. (1978) The effects of feral goats (Capra hircus) on island ecosystems. Biol. Conserv. 13, 279–286 29 Laughrin, L. et al. (1994) Trends in vegetation changes with removal of feral animal grazing pressures on Santa Catalina Island. In The Fourth California Islands Symposium: Update on the Status of Resources (Halvorson, W.L. and Maender, G.J., eds), pp. 523–530, Santa Barbara Museum of Natural History 30 North, S.G. et al. (1994) Changes in the vegetation and reptile populations on Round Island, Mauritius, following eradication of rabbits. Biol. Conserv. 67, 21–28 31 Morris, I. (1996) Kakadu National Park, Australia, Steve Parish Publishing 32 Scowcroft, P.G. and Conrad, C.E. (1992) Alien and native plant response to release from feral sheep browsing on Mauna Kea. In Alien Plant Invasions in Native Ecosystems of Hawai’i: Management and Research (Stone, C.P. et al., eds), pp. 625–665, University of Hawai’i Cooperative National Park Resources Studies Unit 33 Stone, C.P. et al. (1992) Responses of Hawaiian ecosystems to removal of feral pigs and goats. In Alien Plant Invasions in Native Ecosystems of Hawai’i: Management and Research (Stone, C.P. et al., eds), pp. 666–704, University of Hawai’i Cooperative National Park Resources Studies Unit 34 D’Antonio, C.M. and Vitousek, P.M. (1992) Biological invasions by exotic grasses, the References a Courchamp, F. et al. (1999) Cats protecting birds: modelling the mesopredator release effect. J. Anim. Ecol. 68, 282–292 b Pace, M.L. et al. (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol. Evol. 14, 483–488 35 36 37 38 39 40 41 42 43 44 45 46 47 grass/fire cycle, and global change. Ann. Rev. Ecol. Syst. 23, 63–87 Copson, G. and Whinam, J. (1998) Response of vegetation on subantarctic Macquarie Island to reduced rabbit grazing. Aust. J. Bot. 46, 15–24 Klinger, R.C. et al. (1994) Vegetation response to the removal of feral sheep from Santa Cruz Island. In The Fourth California Islands Symposium: Update on the Status of Resources (Halvorson, W.L. and Maender, G.J., eds), pp. 341–350, Santa Barbara Museum of Natural History Wenner, A.M. and Thorp, R.W. (1994) Removal of feral honey bee (Apis mellifera) colonies from Santa Cruz Island. In The Fourth California Islands Symposium: Update on the Status of Resources (Halvorson, W.L. and Maender, G.J., eds), pp. 513–522, Santa Barbara Museum of Natural History Wehtje, W. (1994) Response of a Bishop pine (Pinus muricata) population to removal of feral sheep on Santa Cruz Island, California. In The Fourth California Islands Symposium: Update on the Status of Resources (Halvorson, W.L. and Maender, G.J., eds), pp. 331–340, Santa Barbara Museum of Natural History Wenner, A.M. et al. (2000) Removal of European honeybees from the Santa Cruz Island ecosystem. In Proceedings of the Fifth California Island Symposium (Browne, D.H. et al., eds), Santa Barbara Museum of Natural History Merlin, M.D. and Juvik, J.O. (1992) Relationships among native and alien plants on Pacific islands with and without significant human disturbance and feral ungulates. In Alien Plant Invasions in Native Ecosystems of Hawai’i: Management and Research (Stone, C.P. et al., eds), pp. 597–624, University of Hawai’i Cooperative National Park Resources Studies Unit Eckhardt, R.C. (1972) Introduced plants and animals in the Galapagos Islands. Bioscience 22, 587–590 Rutherford, C. and Chaney, S. (1999) Island plants gain new lease on life. Fremontia 27, 3–5 Van Riel, P. et al. (2000) Eradication of exotic species. Trends Ecol. Evol. 15, 515 Murphy, E.C. et al. (1998) Effects of rat-poisoning operations on abundance and diet of mustelids in New Zealand podocarp forests. N. Z. J. Zoology 25, 315–328 Fischer, J. and Lindenmayer, D.B. (2000) An assessment of the published results of animal relocations. Biol. Conserv. 96, 1–11 Short, J. et al. (1992) Reintroductions of macropods (Marsupialia, Macropodoidea) in Australia: a review. Biol. Conserv. 62, 189–204 Hobbs, R.J. (1999) Restoration of disturbed ecosystems. In Restoration of Disturbed Ecosystems (Walker, L., ed.), pp. 673–687, Elsevier Science Ecología General Trabajo Práctico 9 ESTUDIO DE LA INVASIÓN DE ARDILLAS EN BUENOS AIRES Por RUBEL DIANA; FISCHER SYLVIA; THOMPSON GUSTAVO; LOETTI VERÓNICA OBJETIVOS - Que los alumnos puedan aplicar los modelos de crecimiento poblacional en el contexto de la problemática de las invasiones biológicas. - Introducir a los alumnos en los conceptos básicos de la ecología del paisaje. INTRODUCCIÓN Un caso de invasión biológica que se ha estudiado desde etapas relativamente tempranas, es el caso de la ardilla de vientre rojo, Callosciurus erythraeus (Pallas, 1779) en la provincia de Buenos Aires. Esta ardilla es un roedor arborícola y diurno de tamaño medio (Phylum: Chordata, Clase: Mammalia, Orden: Rodentia, Familia: Sciuridae) originario del noreste asiático (Bangladesh; Camboya; China; India; Laos; Malasia; Birmania; Taiwán; Tailandia y Vietnam). No presenta dimorfismo sexual de tamaño ni pelaje, y la coloración típica del pelaje es marrón oliváceo con una banda negra en el dorso que normalmente se extiende desde la base de la cola hasta la cruz (Cassini & Guichón, 2009). El área de influencia media por individuo en su área de distribución original varía entre 0,3 ha y 0,5 ha para las hembras y entre 1,4 ha a 2,2 ha para los machos (Tamura et al., 1989. En CABI, 2011). Su alimentación es variada, se alimenta de diferentes partes de especies de plantas y también de hongos, insectos, huevos y caracoles. El hábitat en su área de distribución natural consiste principalmente en bosques subtropicales, aunque en China también está presente en bosques subalpinos de coníferas o en bosques mixtos de coníferas y frondosas en altitudes superiores a los 3000 m sobre el nivel del mar (Smith and Xie 2008, en UICN 2011). En Taiwán habita desde bosques de bambú de las zonas bajas hasta los bosques de coníferas que llegan a 3000 m s.n.m. (Hu y Yie, 1970). Dado que esta ardilla es una especie invasora en Japón, Francia, Bélgica, Holanda y Argentina, en las áreas de introducción se localiza en varios tipos de áreas arboladas (bosques naturales, plantaciones de coníferas, cultivos, arbustos y parques urbanos) pero prefiere zonas mixtas de frondosas en Japón (Okubo et al., 2005, en CABI, 2011) y Francia. La invasión en Argentina La invasión se origina en la localidad de Jáuregui, cuando son liberados unos pocos ejemplares por no adaptarse al cautiverio en el que los mantenía un poblador. Guichón y Doncaster (2008) proponen un modelo espacialmente explícito que predice el comportamiento de la invasión de esta especie en nuestro país a partir de la liberación, y los datos que usaremos en el trabajo práctico se basan en dicho modelo, aunque se han simplificado para fines didácticos. Al igual que en el modelo propuesto por Guichón y Doncaster (2008), se tomaron cuatro categorías de hábitat - pastizal, urbano, suburbano y bosque - con diferente capacidad de carga para la población de ardillas, que se presentan en el mapa de la Figura 1 para el área de liberación y sus alrededores. La información demográfica sobre esta población se presenta en la Tabla 1, en tanto que la información sobre el comportamiento de dispersión se puede observar en la Tabla 2. Propuesta de trabajo En base a la información disponible, la propuesta es modelar la invasión en las décadas siguientes a la liberación de los dos primeros ejemplares. Más específicamente predecir cuál será el estado de la población en cuanto al tamaño poblacional y el área de distribución, después de 30 años de la liberación de los primeros ejemplares. Para ello, contarán con el mapa que figura en el anexo, y les proponemos utilizar como guía el cuestionario que sigue y los datos poblacionales que figuran en las Tablas 1 y 2. 28 Ecología General a) ¿Cuál es la capacidad de carga estimada para el parche en el que se produce la liberación inicial de ardillas? b) ¿Cuánto tiempo llevará que la población alcance la capacidad de carga del parche? c) ¿En cuánto tiempo se espera que comience la colonización de nuevos parches? d) ¿Cuál es el escenario esperado en 30 años? ¿Qué población total de ardillas se espera? ¿Qué área de ocupación tendrá la población? e) ¿Qué suposiciones hay que hacer para poder hacer este análisis? f) ¿Qué etapas de la invasión estamos observando en estos análisis? g) Sobre la base a todo lo visto en la clase de hoy: ¿Qué estrategias se podrían proponer para limitar la invasión? Categoría en el mapa Tipo de hábitat Capacidad de carga (ind/ha) Tasa finita de incremento = 1,53/año 0 pastizal 0 1 urbano 2 2 suburbano 4 3 bosque 8 Tabla 1: Información demográfica sobre la ardilla de vientre rojo proporcionada a los alumnos Densidad Nº de parcelas desfavorables que puede cruzar Metros de pastizal que pueden recorrer Menos de 50% de K 0 (no se dispersa) 0 Entre 50% y 75% de K 1 Entre 75% y 90% de K 2 Más de 90% de K 3 100 200 300 Tabla 2: Datos sobre el comportamiento de dispersión. K representa la capacidad de carga. Se supuso que los parches eran colonizados por 4 individuos. Bibliografía Cassini G and Guichón ML, 2009. Variaciones morfológicas y diagnosis de la ardilla de vientre rojo, Callosciurus erythraeus (Pallas, 1779), en Argentina. Mastozoología Neotropical 16(1):39-47. Guichón ML and Doncaster CP, 2008. Invasion dynamics of an introduced squirrel in Argentina. Ecography 31:211-220. Hu Y and Yie ST, 1970. Some biological notes on the Taiwan squirrel. Plant Protection Bull. Vol. 12, No. 1:21-30 (In Chinese). Okubo M, Hobo T and Tamura N, 2005. Vegetation types selected by alien Formosan squirrel in Kanagawa Prefecture. Natural History Report of Kanagawa 26: 53-56. Smith and Xie, 2008 citado en: http://www.iucnredlist.org/details/136490/0 Tamura N, Hayashi F, Miyashita K, 1989. Spacing and kinship in the Formosan squirrel living in different habitats, Oecologia 79:344-352. 29 Ecología General Trabajo práctico 10 PATRONES ESPACIALES Y ESCALAS OBJETIVO GENERAL Analizar la estructura espacial de la heterogeneidad y el efecto de la escala sobre la percepción de la heterogeneidad en un gradiente urbano-suburbano. INTRODUCCIÓN Los sistemas naturales son heterogéneos, y esta heterogeneidad puede darse a distintas escalas espaciales. A una escala dada, la heterogeneidad puede formar distintos patrones: si el ambiente va cambiando en forma continua y gradual a lo largo del espacio hablamos de gradiente, cuando las porciones distintas se ubican en forma contigua, de mosaico ambiental, mientras que si podemos distinguir porciones distintas dentro de un ambiente predominante, se habla de una estructura de parche- matriz (Figura 1). Esta estructura espacial, es decir, cómo se distribuye la heterogeneidad en el espacio, está determinada principalmente por la heterogeneidad del sustrato (por ejemplo, un gradiente de altura, o distintos tipos de suelo), por disturbios naturales (por ejemplo, inundaciones periódicas, incendios) o por las actividades humanas (uso de la tierra, urbanizaciones). a b Figura 1. Esquemas de patrones de heterogeneidad: (a) parches dentro de una matriz, (b) mosaico ambiental La ecología del paisaje es la rama de la ecología que estudia cómo la estructura espacial afecta los procesos ecológicos y, a su vez, cómo estos procesos determinan la estructura espacial. Un paisaje está formado por un conjunto de ecosistemas que se repiten en el espacio (a una escala de entre 10 y 100 km de diámetro), y puede ser descripto por sus elementos: tipos, forma y tamaño de parches, forma, longitud y ancho de corredores, y tipo de matriz. La matriz es el tipo de parche más frecuente, y puede ser más o menos extensa, dispersa o agregada, y estar más o menos perforada. Por otro lado, un paisaje también se caracteriza por el arreglo espacial de los elementos (grado de agregación) y el grado de diferencia entre los distintos tipos de parches (contraste), Figura 2. Un conjunto de paisajes forma una región, que es un área geográfica mayor determinada por sus características geológicas, el macroclima y una actividad humana común, sus distintas partes están conectadas por transporte, comunicación y cultura. Tanto los paisajes como las regiones son escalas espaciales “humanas”, no corresponden a niveles de organización biológica. Como hemos dicho antes, las características y los procesos que suceden a escala de paisaje están determinados por sus elementos, es decir, por las características y procesos a una escala menor. Pero también están influidas por las características de la región donde están inmersos los paisajes. Es decir, lo que sucede a una escala dada, está determinada por los niveles superiores e inferiores. 30 Ecología General Poca agregación Mucha agregación Poco contraste Mucho contraste Figura 2. Componentes de la heterogeneidad: contraste y agregación Según la escala en que estemos trabajando, vamos a poder distinguir la heterogeneidad a distintos niveles, como cuando se cambia el aumento de un microscopio cambian los detalles de algunas estructuras, o cuando un avión se va acercando a tierra va cambiando el nivel de detalle con que uno ve los objetos, pero dejamos de percibir otros niveles de heterogeneidad a mayor escala. Por otro lado, según el ambiente, la heterogeneidad puede variar según la escala de observación debido al tamaño de los parches. Si los parches son muy grandes (grano grueso, Figura 3) trabajar en una escala pequeña (de detalle) no los percibimos debido a que abarcamos un solo tipo de parche, mientras que si los parches son pequeños (grano fino, Figura 3) al trabajar a escalas grandes no son distinguibles. Grano grueso Grano fino Figura 3. Grano de un paisaje de acuerdo al tamaño promedio de los parches 31 Ecología General Es importante diferenciar entre la escala ecológica y la escala cartográfica. Esta última se refiere a la relación entre la distancia que hay entre dos puntos dados en su representación en un mapa respecto a su distancia real (Por ejemplo 1:50000, 1:250000). La escala ecológica se refiere a la dimensión espacial y/o temporal de un objeto o proceso. Un proceso de gran escala abarca un área grande y/o dura un tiempo largo (por ejemplo, las glaciaciones ocuparon grandes áreas y se produjeron durante largos períodos de tiempo). Por otro lado, un proceso a pequeña escala ocurre en dimensiones limitadas o en tiempos relativamente cortos (por ejemplo, perturbación producida por la caída de un árbol). La escala se distingue por su grano y su extensión. El grano es el tamaño de la mínima unidad distinguible (como el tamaño de los granos de arena o la rugosidad de una lija) y la extensión es el tamaño total abarcado (Figura 4). Si uno está parado en un punto, hasta dónde puede abarcar con la vista sería la extensión y los detalles que puede percibir son el grano. Entre ambos puede haber un número variable de niveles intermedios. El grano y la extensión dependen de las características de cada especie, principalmente su tamaño y movilidad. Las especies más grandes y/o que recorren mayores distancias tienden a tener una extensión mayor que las especies pequeñas y sedentarias. Extensión Grano Figura 4: Para un organismo dado, la extensión es el mayor tamaño al que puede distinguir la heterogeneidad, el grano el menor tamaño. En la figura se distinguen 3 niveles, los parches más chicos representan el grano y el área más grande representa la extensión. DESARROLLO Área de estudio: En este trabajo práctico vamos a analizar el efecto de los cambios de escala en la percepción de la heterogeneidad en la región metropolitana de Buenos Aires y alrededores, hasta la zona del Río Luján- Otamendi, Partido de Campana. Se tratará de determinar a cada escala los factores que determinan la heterogeneidad, teniendo en cuenta que ésta es el resultado y la expresión de procesos que actúan a distintas escalas y son de distinto origen, en particular en la región estudiada, la heterogeneidad observada resulta de la interacción entre procesos naturales y las transformaciones que introduce el hombre al hacer uso del suelo. El área estudiada comprende un mosaico de comunidades donde están representadas tres ecorregiones determinadas principalmente por el clima y la topografía: la ecorregión Delta e Islas del Paraná, representada por el bosque ribereño, la región Pampeana, representada por los pastizales de la zona alta, y la región del Espinal, representada por los talares que se desarrollan sobre albardones de conchilla en la barranca. La ecorregión Delta e Islas del Paraná corresponde a los valles de inundación de los trayectos medios e inferiores de los río Paraná y Paraguay, e incluye al 32 Ecología General Delta del Paraná. Se trata de un paisaje de islas bajas e inundables. La ecorregión de la Pampa constituye el sistema de praderas más importante de la Argentina. Su relieve es relativamente plano y está expuesta a anegamientos permanentes o cíclicos. Las praderas estuvieron originalmente dominadas por gramíneas entre las que predominaron las del género Poa, Stipa, Piptochaetiun y Aristida. Es la ecorregión que más transformación ha sufrido debido a procesos de urbanización y a la implementación de la agricultura y ganadería extensiva. El Espinal desde el punto de vista arbóreo está caracterizado por la presencia del género Prosopis (algarrobos, ñandubay y caldén). En la provincia de Buenos Aires los talares son los representantes típicos del espinal. Pamp Delta Costa Río AMBA Costa Pampa Figura 5. Unidades del paisaje en la región metropolitana de Buenos Aires Las características propias de cada ecorregión han sido modificadas por las actividades humanas, dando lugar en el área a cinco grandes unidades de paisaje en la Región Metropolitana (Atlas Ambiental de Buenos Aires; Figura 5): • • • • • La Planicie Pampeana y la Franja Costera ocupada por la urbanización, a la que se denomina Área Metropolitana de Buenos Aires (AMBA) La Planicie Pampeana no ocupada por la urbanización, a la que se denomina Pampa La Franja Costera no ocupada por la urbanización, a la que se denomina Costa El Bajo Delta del Río Paraná, que se denomina Delta El Estuario del Río de la Plata que se denomina Río La división entre el AMBA y la Pampa es dinámica y arbitraria, y entre ellas se presenta una interfase, comúnmente denominada “periurbano”, en la cual se registran simultáneamente manifestaciones urbanas y rurales. Durante los últimos años, la Región Metropolitana de Buenos Aires ha experimentado una intensa transformación del territorio y de los usos dominantes. Por ejemplo, en algunos sectores de los valles de inundación de los ríos Luján, Reconquista y Paraná de las Palmas puede observarse que amplios sectores de la franja periurbana y de numerosos espacios intersticiales han pasado de un uso rural a otro urbano, especialmente residencial, recreativo y comercial. Extendiéndose más hacia el norte de la Región Metropolitana, donde disminuye la urbanización, se puede distinguir la transición de los pastizales en la zona alta hacia los talares de la barranca, los 33 Ecología General humedales en la zona baja hasta la selva en galería a lo largo de arroyos y del río Paraná. En esta zona tenemos representadas comunidades vegetales asociadas tanto a ambientes terrestres como a ambientes acuáticos. Podemos encontrar diferentes comunidades de herbáceas, bosques, ríos, arroyos y canales. A pequeña escala no es el clima el que determina el desarrollo de diferentes comunidades vegetales, sino que los factores principales son la hidrología y el tipo de suelo, ambos asociados al relieve (presencia de barrancas, zonas de inundación) y microrelieve. Las comunidades terrestres que se desarrollan en cada zona dependen del relieve y las características físico–químicas del suelo (principalmente la salinidad y la humedad), nivel de la napa freática, frecuencia de inundaciones y período durante el cual el suelo permanece inundado. Puede observarse, entonces, un gradiente de las comunidades vegetales asociado al relieve y a la hidrología (Figura 6). Parte baja del humedal Talar Pastizal Figura 6. Esquema de localización de las diferentes comunidades según su posición en la barranca de río Desarrollo del Trabajo Práctico: Trabajo en laboratorio con GoogleEarth: Describir la heterogeneidad espacial a distintas escalas cartográficas e identificar los distintos elementos que se pueden distinguir en cada caso. Google Earth es un programa informático que existe bajo este nombre desde mayo 2005 y que permite visualizar el planeta entero a través de un mosaico de imágenes de satélite o fotografías aéreas. El programa permite visualizar la superficie terrestre desde diferentes alturas, lo que implica diferentes escalas de la imagen que se obtiene. Actividades: 1) Descripción de la estructura del paisaje a distintas escalas en tres puntos ubicados a distancia creciente de la ciudad de Buenos Aires: Se trabajará con los puntos geográficos 1 y 5 especificados en la Tabla 1. Para ubicarlos en el mapa debe escribir las coordenadas geográficas en el recuadro que dice “volar a” del Google Earth (recordar que latitud Sur y longitud Oeste se representan con valores negativos). En cada punto se trabajará a tres escalas diferentes. Para ello se ubicará el punto en el centro de la pantalla y se buscará que la escala que muestra el Google Earth en el extremo inferior izquierdo, coincida con 4 km, 1 km y 100 m. Para cada punto y a cada escala especificar: Tipos de unidades distintas que se distinguen, tamaño promedio de las unidades, proporción del área con cada unidad y contraste entre unidades. Comparar los distintos puntos en cuanto a la heterogeneidad, y a cómo varía ésta según la escala. Los criterios a usar para identificar las unidades de paisaje, así como los distintos ambientes son: la forma, el color y la textura de la imagen. 2) Descripción de la estructura del paisaje a lo largo de una transecta que va desde la ciudad de Buenos Aires hacia el norte, abarcando unos 50 km. hasta la zona del río Luján: 34 Ecología General Los cinco puntos especificados en la Tabla 1 se encuentran a lo largo de una transecta. Se ubicarán esos puntos en el mapa a partir de sus coordenadas y se visualizará la transecta. Luego se trabajará con cada uno de ellos a una escala 1:1000, analizando una superficie de aproximadamente 4 Km2 (2 X 2 Km). Para cada punto se cuantificará sobre la imagen de Google Earth la composición relativa de distintos componentes del paisaje, y los resultados serán volcados en la planilla adjunta (Tabla 2). Tabla 1. Localización de los puntos a observar durante el trabajo práctico Punto 1 Localización de los puntos Tercer puente después de tomar Panamericana Latitud -34.533176° Longitud -58.502494° Punto 2 Bifurcación del ramal tigre, justo pasando el primer puente. Latitud -34.488707° Longitud -58.570718° Punto 3 Panamericana y Ruta 197 Latitud -34.474717° Longitud -58.661775° Punto 4 Punto 5 Punto 6 Av. Benavidez (Ruta 27). Latitud -34.420476° Longitud -58.717830° Primer puente peatonal después del arroyo escobar. Latitud -34.367515° Longitud -58.774746° Cruzando el Río Luján, aproximadamente km 60 Latitud -34.295539° Longitud -58.884219° Tabla 2. Planilla para describir la estructura del paisaje en los 6 puntos a lo largo de la transecta Buenos Aires–Río Luján. Punto 1 Tipos de uso de la tierra a) % Residencial (total) a1) % Viviendas multifamiliares (edificios y departamentos) a2) % Viviendas unifamiliares (casas y ph) a3) % Barrios cerrados, countries b) % Industrial/Comercial (incluye: escuelas, cementerios, clubes, etc) c) % Espacios verdes no naturales/ parques (no pertenecientes a countries) d) % de terreno agrícola e) % de terreno natural o no agrícola (pasturas, pastizales naturales) f) % de rutas o autopistas Otros indicadores % total de la superficie construida o pavimentada (sin incluir calles o rutas) % total de la superficie con vegetación N° de cuadrados con rutas o caminos 35 Punto 2 Punto 3 Punto 4 Punto 5 Punto 6 Ecología General BIBLIOGRAFÍA Atlas Ambiental de Buenos Aires. http://www.atlasdebuenosaires.gov.ar/aaba Begon, M., Harper, J.L.& Towsend, C.R. 1987. Ecología: Individuos, poblaciones y comunidades. De. Omega, Barcelona. Bonfilds, C. G. 1962. Los suelos del Delta del río Paraná. Factores generadores, clasificación y uso. INTA (RIA). Num. 16 (3) 370 pp. Buenos Aires. Bonfilds, C. G. 1962. Los suelos del Delta del río Paraná. Factores generadores, clasificación y uso. INTA (RIA). Num. 16 (3) 370 pp. Buenos Aires. Brown A., Martínez Ortíz U., Acerbi M., Corcuera J., 2005. La situación ambiental argentina 2005. Fundación vida silvestre argentina. Chichizola S., 1993. Las comunidades vegetales de la Reserva Natural Estricta Otamendi y sus relaciones con el ambiente. Parodiana 8 (2): 227-263. Forman RTT, (1999) Landscape ecology, the growing foundation in landuse planning and naturalresource management. In: Kovar P (Ed.) Nature and culture in landscape Iriondo MH y Scotta E. 1978. The evolution of the Paraná River Delta. Proceedings of the International Symposium on coastal Evolution in the Quaternary: 405-418. INQUA,San Pablo, Brasil Kandus P., Malvárez A.I. y N. Madanes. 2003. Estudio de las comunidades de Plantas Naturales de las Islas del Bajo Delta del Río Paraná. (Argentina). Darwiniana 41 (1-4): 1-16. Nacional.ISSN 00116793 Kandus P., Quintana R D., Bó R., 2006. Patrones de paisaje y biodiversidad del bajo delta del río Paraná. http://www.ambiente.gov.ar/default.asp?IdArticulo=5505 Krebs, Charles, J. 1986. Ecología. Análisis experimental de la distribución y abundancia. Ed. Pirámide. Madrid. Madanes, N. 2008. Humedales de la Reserva Natural Otamendi. En Guía de la Flora de la Reserva Natural Otamendi. Editora Liliana Goveto. Publicación de la Administración de Parques Nacionales. En prensa Malvárez, A.I y R.F. Bó. 2002. Cambios ecológicos en el Delta Medio del Río Paraná debidos al evento de El Niño 1982-1983”. Publicación especial del Taller “El Niño, sus impactos en el Plata y en la Región Pampeana. J.A. Schnack (Ed.). La Plata, Buenos Aires. Marchetti B, Ruiz L., Madanes N., Sartori G. y P. Cichero. 1988. Relevamiento del medio natural y una propuesta de plan de manejo para la futura Area Natural Protegida " Ing. Rómulo Otamendi". Informe Interno Administración Parques Nacionales: 1-53. Biblioteca Administración de Parques Nacionales Matteucci, S. y Colma A. 1982. Metodología para el estudio de la vegetación. O.E.A. Serie de Biología. Matteucci, Silvia D.; Jorge Morello; Gustavo D. Buzai; Claudia A. Baxendale; Mariana Silva; Nora Mendoza; Walter Pengue y Andrea Rodríguez. 2006. Crecimiento urbano y sus consecuencias sobre el entorno rural. Orientación Gráfica Editora. Buenos Aires. (350 páginas).ISBN 978-9879260-45-6 36 Ecología General DEJAR ESTA HOJA EN BLANCO 37 Trabajo práctico 10 - Patrones espaciales y escalas TURNO: Punto/altura GRUPO: Extension aproximada Tipo de elemento Caracterizacion Proporcion de (metros cuadrados) (matriz, parche, corredor) (nombre que le pondrian) cobertura 1/4 km 1/ 1 km 1/ 250 m 5/4 km 5/ 1 km 5/ 250 m 38 Ecología General DEJAR ESTA HOJA EN BLANCO 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 1 0 0 0 0 0 0 0 0 0 2 2 2 2 1 1 1 1 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 MAPA ARDILLAS 5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 6 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 7 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 8 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 9 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 10 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 11 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 12 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 13 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 14 2 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 15 2 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 3 3 3 3 3 16 2 2 2 2 2 2 2 0 0 0 0 0 0 0 3 3 3 3 3 3 3 17 1 1 1 2 2 2 2 2 0 0 0 0 0 0 0 3 3 3 3 3 3 18 1 1 1 2 2 2 2 2 0 0 0 0 0 0 0 3 3 3 3 3 3 19 1 1 1 2 2 2 2 2 0 0 0 0 0 0 0 0 3 3 3 3 0 20 1 1 1 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 21 1 1 1 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 22 1 1 1 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 2 23 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 24 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 25 0 0 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 26 0 0 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 27 0 0 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 28 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 29 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 30 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 31 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 32 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 2 0 33 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 2 2 2 2 2 34 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 2 2 2 2 35 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 3 2 1 1 1 36 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 3 2 1 1 1 Las cuadrículas se asignaron a una categoría cuando más del 50% de la superficie correspondió al habitat de la categoría La cuadrícula es de 100m x 100 m X Punto de liberación de los primeros ejemplares. 0 Pastizal 1 Urbano 2 Suburbano 3 Bosque 37 3 3 3 3 3 3 3 2 2 2 2 2 2 2 2 2 2 2 2 1 1 38 3 3 3 3 3 3 3 2 2 2 2 2 2 2 2 2 2 2 2 1 2 39 3 3 3 3 3 3 3 3 3 3 2 2 2 2 2 2 2 2 2 2 2 40 3 3 3 3 3 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 41 3 3 3 3 3 3 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 42 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 0 0 0 Ecología General 39 Ecología General DEJAR ESTA HOJA EN BLANCO 40 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 2 2 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 2 2 1 1 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 2 1 1 1 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 1 1 1 1 1 1 2 2 2 2 2 3 3 3 3 0 0 0 3 3 0 3 0 0 0 0 0 0 0 0 1 1 1 X 1 1 2 2 2 2 2 2 3 3 3 0 0 3 0 0 0 3 0 0 0 0 0 0 0 0 1 1 1 1 1 1 2 2 2 2 2 2 2 3 3 0 3 0 0 0 0 3 0 0 0 0 0 0 0 0 1 1 1 1 1 1 2 2 2 2 2 3 3 3 3 0 0 0 0 0 0 3 0 0 0 3 2 2 2 2 2 1 1 2 2 1 2 2 2 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 3 2 2 2 2 2 2 1 2 2 1 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 3 3 2 2 2 2 0 0 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 3 3 3 2 2 3 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 3 3 3 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 3 3 3 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 2 3 2 2 2 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 2 2 2 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 2 2 2 2 2 1 1 1 2 2 3 3 3 2 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 2 2 2 0 2 1 1 1 2 2 2 2 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 2 2 2 2 2 2 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 2 2 2 2 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 2 2 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 3 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Ecología General 41 Ecología General DEJAR ESTA HOJA EN BLANCO 42 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 0 0 0 0 0 0 0 2 2 2 2 2 2 2 0 0 0 0 0 0 0 0 0 0 3 3 0 3 3 0 0 0 0 0 0 0 2 2 1 1 1 1 2 2 2 0 0 0 0 3 3 3 3 3 3 3 0 3 0 0 0 0 0 0 0 2 1 1 1 1 1 2 2 2 3 3 3 3 3 3 3 3 3 3 3 3 3 0 0 0 0 0 0 0 2 2 1 1 2 2 2 2 3 3 3 3 3 3 3 3 3 3 3 3 3 3 0 0 0 0 0 0 0 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 3 0 0 0 0 0 0 0 0 3 0 0 0 2 2 2 2 2 2 3 3 3 3 3 3 3 3 3 3 3 0 0 0 0 0 0 0 3 3 0 0 0 2 2 2 0 0 0 0 0 0 0 3 3 3 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 3 3 3 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Ecología General 43 Ecología General 46 Ecología General arriba-izquierda] B C A C G A A F B B B A K E A B M E C G D I J A B E L A N A D A F A G A A A A B A B E L H D D E C G G I I G F D F C D H H I H A B F G B A A I A D N A G F G H B A J A B E G B D B B F F C A B E I C B J M C C C E D G B J B A A L C A B J B J A J A J i 47 H J A H B A C C A H C A C C H A C G I C A C D D A G K D B A A B L J N L C H E C L C E J D G C C C A C C C G G J J L A F C J A B G B M C G A J A A C N J A H C C A F J J D E A B I B B D A A I D G N B L B B M G J I F E E B B A D B A J B B B A B A A G A M B C C A A A B L C G D A A A G A B Ecología General DEJAR ESTA HOJA EN BLANCO 48 Ecología General D B G A A A A A B D E B E B A D C A A C A A C C B D D C C C C A C C A C B C C C A C C C C E E C C C C A C C A B C B C C E C A A C C C [arriba-derecha] B A J D B B A B A A B D A A C A I I A I B E A E A B C A D B N A C A B A A A D C J J C J B C B A C M A E E B D A K B B A A C J C F C K B A C A J C H ii 49 A A B G B A C B A A C A B B B A B A C D G G J J G K C A H A B B J K B A J B B E B A A C C A C A B C E A L I A B B A N A C C A C J C C B C B D C D J A J B A B B A A B A J A G A A B G D B C C B B Ecología General DEJAR ESTA HOJA EN BLANCO 50 Ecología General i G A B H L M G A A A A A B B A A B B B A B E D F J A G D J E M A A D B A A D A B D M I A M A A J I D D C F B B L A B E F N G A A B J A A G G H A E A B N B B I F A F A E I A A F F L A J E B B F B I E F E J H E B K E H [abajo-izquierda] 51 F M A B A B E D A A F M E B F I I A A G A E L E A B E A E M K I B B B A F A J I A E F G B N N A B L G D A I A A A B J A B H A I G D F B G M B B B A I H A A F B E A D E L A B C B B B H L F G I A J D D B A B H D C A A D A A A F E A D I Ecología General DEJAR ESTA HOJA EN BLANCO 52 Ecología General ii B J J J A A A D B A A A A B J A B J A I A J A A A E A B E A F I A A I A E A A A A A A D A B B A F E E E B A I G [abajo-derecha] 53 E M E G E A M E F E A F E M F F E E E J A A I F L A F M A A B N F A B I I A K B A A F A M L A M A A A F A B J A A J L A A F A B J E A A E E A