Ecologia General Guia TP 2016 parte 2

Transcripción

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.
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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.
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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.
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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.*
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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)
-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)
-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
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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
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Seguridad en laboratorios de docencia (
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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
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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).
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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?
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Figura 1: Tamaños sucesivos de muestreador para la evaluación del área mínima.
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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:
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(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
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
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
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].
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
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
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
Number of exotic species
174
Number of native species
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
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
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
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
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
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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
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
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
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.
(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
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:
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
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
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
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)
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
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
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.
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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
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40
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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
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.
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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.
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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
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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
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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
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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:
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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.
Punto 3
Panamericana y Ruta 197
Punto 4
Punto 5
Punto 6
Av. Benavidez (Ruta 27).
Primer puente peatonal después del arroyo escobar.
Cruzando el Río Luján, aproximadamente km 60
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
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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".
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Nacionales
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Biología.
Matteucci, Silvia D.; Jorge Morello; Gustavo D. Buzai; Claudia A. Baxendale; Mariana Silva; Nora
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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
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
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
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
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0
0
0
0
0
0
0
0
0
0
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0
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0
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0
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0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
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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
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0
0
3
3
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0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
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0
0
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3
0
0
0
0
0
0
0
0
0
0
0
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0
0
0
0
0
0
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0
0
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0
0
0
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0
0
0
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0
0
0
0
0
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0
0
0
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0
0
0
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0
0
0
0
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0
0
0
0
0
0
0
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0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
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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
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0
0
0
0
0
0
0
0
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0
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0
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0
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0
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0
0
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0
0
0
0
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0
0
0
0
0
0
0
0
0
0
0
0
0
0
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3
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0
0
0
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
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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
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0
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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
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3
3
3
3
3
3
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0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
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3
3
3
3
3
3
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0
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0
0
0
0
0
0
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0
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0
0
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0
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0
0
0
0
0
0
0
0
0
0
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0
0
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0
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3
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3
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0
0
0
0
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0
0
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0
0
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0
0
0
0
0
0
0
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2
2
2
2
2
2
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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
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0
0
0
0
0
0
0
3
3
3
3
3
3
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0
0
0
0
0
0
0
0
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0
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0
0
0
0
0
0
0
0
3
3
3
3
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0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
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0
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
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
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
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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
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

Ecologia General Guia TP 2016 parte 2

Transcripción

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