Population Persistence and Offspring Fitness in the Rare Bellflower Campanula cervicaria in Relation to Population Size and Habitat Quality

Data from several animal species and a few plant species indicate that small populations face an elevated risk of extinction. Plants are still underrepresented in these studies concerning the relation between population size and persistence. We studied the effect of population size on persistence among natural populations of the rare bellflower Campanula cervicaria in Finland. We monitored 52 bellflower populations for 8 years and found that the mean population size decreased from 24 to 14 during this period. Small populations with # 5 individuals were more prone to losing all fertile plants than were larger ones. Reduction in population size was nevertheless unrelated to the degree of population isolation, measured as the distance to the nearest known population. To test the hypothesis that offspring fitness is lower in small populations, we germinated bellflower seeds from different-sized populations in a laboratory and found that seed germination ability was independent of population size. The seedlings raised from seeds of small populations grew faster than those taken from larger populations. Population size was negatively related to the amount of shade in the habitats. In conclusion, decreasing population sizes of C. cervicaria seemed not to be caused by lowered germination ability or growth rate in small populations; rather, population size reductions appeared to be due to closing of vegetation in the habitats. Persistencia Poblacional y Adaptabilidad de Crías en la Especie Rara Campanula cervicaria con Relación al Tamaño Poblacional y la Calidad del Hábitat Resumen: Los datos de varias especies de animales y de unas pocas especies de plantas indican que las poblaciones pequeñas enfrentan un riesgo elevado de extinción. Las plantas están aún menos representadas en estos estudios concernientes a la relación entre el tamaño poblacional y la persistencia. Nosotros estudiamos el efecto del tamaño poblacional sobre la persistencia de poblaciones naturales de la rara Campanula cervicaria en Finlandia. Monitoreamos 52 poblaciones de C. cervicaria por 8 años y encontramos que el tamaño promedio poblacional disminuyó de 24 a 14 durante este período. Las poblaciones pequeñas con # 5 individuos fueron más propensas a perder todas las plantas fértiles que las poblaciones grandes. Sin embargo, la reducción en el tamaño poblacional no estuvo relacionada con el grado de aislamiento poblacional, medido como la distancia a la población más cercana. Para evaluar la hipótesis de que la adaptabilidad de la progenie es menor en poblaciones pequeñas, germinamos semillas de C. cervicaria de diferentes tamaños poblacionales en un laboratorio y encontramos que la germinación de semillas fue independiente del tamaño poblacional. Las plántulas provenientes de poblaciones pequeñas crecieron más rápido que aquéllas tomadas de poblaciones más grandes. El tamaño poblacional estuvo negativamente relacionado con la cantidad de sombra en los hábitats. En conclusión, la disminución del tamaño poblacional de C. cervicaria aparente§ Address correspondence to P.M. Tikka, email [email protected] * The names of the authors are presented in alphabetical order. Paper submitted June 7, 1999; revised manuscript accepted December 28, 1999. 1414 Persistence, Fitness, and Population Size in Campanula cervicaria Eisto et al. Conservation Biology Volume 14, No. 5, October 2000 Introduction Destruction, fragmentation, and degradation of the environment often create small and isolated populations (Andrén 1994; Meffe & Carroll 1997), and small populations are more prone to extinction than larger ones (Shaffer 1981; Schoener & Spiller 1992; Ouborg 1993; Lynch et al. 1995). An elevated risk of local extinction is connected to the fact that demographic, genetic, and environmental stochasticity affect small populations more severely than larger populations (Lande 1988; Ellstrand 1992; Primack 1993; Gomulkiewicz & Holt 1995; Groom 1998). The role and significance of these stochastic events, however, vary greatly between taxa and populations. An association between small population size and an increased risk of extinction is more often reported for animals (Diamond 1984; Schoener & Spiller 1987, 1992; Pimm et al. 1988; Hanski et al. 1995) than for plants (Ouborg 1993; Newman & Pilson 1997). Small and fragmented plant populations, however, are presumed less viable than larger ones because of related processes such as the loss of genetic polymorphism (Karron 1987; Raijmann et al. 1994), inbreeding depression (Ellstrand & Elam 1993), and reduced pollination success ( Jennersten & Nilsson 1993; Ågren 1996; Kearns & Inouye 1997). Genetic, environmental, and management factors can also have combined effects on population viability that are not detectable if analyzed independently (Menges & Dolan 1998). In northern Europe, one group of plants exhibiting a dramatic decline in population numbers and size are species typical of seminatural grasslands. Their habitats have become scarce and isolated as a consequence of reforestation, transformation to arable fields, and cessation of hay making, grazing, and clearing by burning. In Finland as much as 25% of the plant species under threat have their optimal occurrence in seminatural grasslands such as meadows, pastures, and glades (Rassi et al. 1992). These species suffer from shading and from competition by tall plants that invade habitats following changes in land use (Armesto & Pickett 1985; Zobel 1992). Many grassland plants, however, have been able to move to alternative, open habitats, such as road and railway verges (Tikka et al. 2000). These habitats may compensate for the isolation of remaining seminatural grasslands and enable their plant populations to form metapopulations in which species persist by moving from destroyed habitat patches to suitable patches nearby (Eriksson 1996). We conducted an extensive, multiyear survey of a rare, monocarpic grassland herb, the bellflower ( Campanula cervicaria L), in Finland. We sought to identify the reasons for its decline and to outline measures for its preservation. As a relatively short-lived, monocarpic species, C. cervicaria has a higher risk of population extinction than perennial or clonal plants (Fischer & Stöcklin 1997). For grassland plants, habitat quality (i.e., openness) is important. We therefore tested the effects of shading by field-layer vegetation, shrubs, and trees on the performance of C. cervicaria populations. We studied the effects of population size and isolation on the shortand longer-term persistence of bellflower populations and tested the hypothesis that offspring fitness of individuals in small populations is lower than that of individuals in larger ones. The results of earlier studies on plant populations either support this prediction (Menges 1991; Heschel & Paige 1995, Fischer & Matthies 1998) or contradict it (Widén 1993; Hauser & Loeschcke 1994; Ouborg & van Treuren 1995; Kunin 1997; Lammi et al. 1999). Moreover, it is a matter of debate at what stage of the reproductive cycle possible effects on fitness are expressed (Widén 1993; Oostermeijer et al. 1994 a ; Waser & Price 1994). The main questions we addressed were as follows: (1) Is the persistence of populations related to population size or degree of isolation? (2) Is there any association between current population size and seed germination ability or the growth of seedlings? (3) Is there any association between former variations in population size and seed germination ability or the growth of seedlings? (4) Are population size, seed germination ability, or growth of seedlings related to the coverage of surrounding vegetation?