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Lagged Effects of North Atlantic Oscillation on Spittlebug Philaenus Spumarius (Homoptera) Abundance and Survival

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Lagged Effects of North Atlantic Oscillation on Spittlebug Philaenus Spumarius (Homoptera) Abundance and Survival Global Change Biology (2006) 12, 2250–2262, doi: 10.1111/j.1365-2486.2006.01266.x Lagged effects of North Atlantic Oscillation on spittlebug Philaenus spumarius (Homoptera) abundance and survival ANTTI HALKKA*, LIISA HALKKA*w ,OLLIHALKKA*w , KAISA ROUKKAw and J U S S I P O K K I w *Department of Biological and Environmental Sciences, University of Helsinki, PO Box 65, 00014, Helsinki, Finland, wTva¨rminne Zoological Station, University of Helsinki, Helsinki, Finland Abstract The North Atlantic Oscillation (NAO) is a large-scale pattern of climate variability that has been shown to have important ecological effects on a wide spectrum of taxa. Studies on terrestrial invertebrates are, however, lacking. We studied climate-connected causes of changes in population sizes in island populations of the spittlebug Philaenus spumarius (L.) (Homoptera). Three populations living in meadows on small Baltic Sea islands were investigated during the years 1970–2005 in Tva¨rminne archipelago, southern Finland. A separate analysis was done on the effects of NAO and local climate variables on spittlebug survival in 1969–1978, for which survival data existed for two islands. We studied survival at two stages of the life cycle: growth rate from females to next year’s instars (probably mostly related to overwintering egg survival), and survival from third instar stage to adult. The latter is connected to mortality caused by desiccation of plants and spittle masses. Higher winter NAO values were consistently associated with smaller population sizes on all three islands. Local climate variables entering the most parsimonious autoregres- sive models of population abundance were April and May mean temperature, May precipitation, an index of May humidity, and mean temperature of the coldest month of the previous winter. High winter NAO values had a clear negative effect on late instar survival in 1969–1978. Even May–June humidity and mean temperature of the coldest month were associated with late instar survival. The climate variables studied (including NAO) had no effect on the growth rate from females to next year’s instars. NAO probably affected the populations primarily in late spring. Cold and snowy winters contribute to later snow melt and greater spring humidity in the meadows. We show that winter NAO has a considerable lagged effect on April and May temperature; even this second lagged effect contributes to differences in humidity. The lagged effect of the winter NAO to spring temperatures covers a large area in northern Europe and has been relatively stationary for 100 years at least in the Baltic area. Keywords: Arctic Oscillation, food plants, humidity, insect, local climate, NAO, North Atlantic Oscillation, Philaenus spumarius, spittlebug, spring temperature Received 6 July 2005; revised version received 1 May 2006 and accepted 5 June 2006 It is generally described by an index depicting sea level Introduction pressure difference between the Arctic and the subtro- The North Atlantic Oscillation (NAO) is the principal pical Atlantic (Hurrell et al., 2003). When the NAO mode of annual to decadal climate variability in the index is positive, westerly winds bring relatively warm extratropical Northern Hemisphere (Hurrell et al., 2003). winter temperatures into northern Europe. A negative mode of the NAO causes the winters to be relatively Correspondence: Antti Halkka, fax 1 358 9 191 57 694, cold. NAO has been repeatedly connected to global e-mail: antti.halkka@helsinki.fi warming in the Northern Hemisphere (Hurrell, 1995); r 2006 The Authors 2250 Journal compilation r 2006 Blackwell Publishing Ltd LAGGED EFFECTS OF NAO 2251 a positive trend in NAO was associated with over ratio typical of the phloem-feeding aphids) (Horsfield, half of the winter surface warming in the Eurasia 1978; Raven, 1983). A xylem feeder is very sensitive to towards the end of the last century (Gillett et al., withering of the food plant. P. spumarius nymphs are 2003). Recently, the winter NAO index has been sensitive to desiccation, both directly and indirectly, and decreasing, and overall trends in the past 30 years in this species thus is a useful indicator of variability of the NAO and the closely related Arctic Oscillation (AO) humidity of its meadow habitats. Tapping of xylem by have been weak or nonexistent (Cohen & Barlow, 2005). spittlebugs can have profound negative effects on the A recent analysis of coupled climate models shows, food plants (Carson & Root, 1999). This top-down effect however, that the NAO may intensify with further probably can be exaggerated when the plants are under increases in greenhouse gas concentrations (Kuzmina stress during dry periods. et al., 2005). Our analysis is based on a long-term study (1969– The number of reports on the effects of the NAO on 2005) of archipelago spittlebug populations in the the phytoplankton, planktonic invertebrates and fishes Tva¨rminne section of the Gulf of Finland archipelago is large and increasing. A considerable body of litera- (Halkka et al., 2001). We investigate the effects of NAO ture even exists on the NAO and terrestrial plants and and selected local climate variables on spittlebug abun- vertebrates in northern Europe (Post & Stenseth, 1999; dance for 1970–2005. The same variables are tested in Forchhammer, 2001; Helle et al., 2001; Ottersen et al., models of spittlebug survival, for which we have data 2001; Stenseth et al., 2002, 2003). for a shorter period (1969–1978). A specific question is In their review of terrestrial ecosystem response to to find out how and when climate has strongest effects NAO variability, Mysterud et al. (2003) found that on the populations and how NAO might be connected nothing had been published on the possible relation- to such climate phenomena. ships between terrestrial invertebrates and NAO. This surprising lack of coverage seems to continue till the Materials and methods present day, although Sparks et al. (2005) showed that high NAO-index values were associated with greater The centre of the study area lies at 591500N, 231150E numbers of overseas migration of Lepidoptera into (indicated as TV in Fig. 4a). The study islands comprise Britain. a part of the western Gulf of Finland archipelago and Insect populations living in tiny meadows on skerries belong to the Tva¨rminne Zoological Station of the of the Baltic Sea offer good opportunities for investiga- University of Helsinki. Two sampling methods for tions on the role of climate in the life of terrestrial collection of the meadow spittlebugs were used, ‘sweep invertebrate populations. The Gulf of Finland archipe- net’ and ‘minicage’ (described in Halkka & Halkka, lago along the north-eastern side of the Baltic Sea is 1990). Both methods were used in such a way that the characterized by numerous low, small rocky skerries sex and colour phenotype of all the captured adult and a smaller number of larger, wooded islands. There individuals were ascertained on the spot, after which is no tide, but south-westerly gales can occasionally the spittlebugs were released into the herbage. Both raise the water level about 1 m above the long-time methods (but on different islands and time periods) average. Tiny meadows on the skerries are sensitive to were used for estimating the sizes of the populations. changes in the physical environment. The soil layer is The sweep net method was used in the years 1970–2005 quite thin and is easily either desiccated or water- in populations on the islands Gulkobben, Rovholmen logged. and Stora Va¨stra La˚nggrundet (SVL). We used the nets Not many species of plants or animals are able to until we observed a strong diminution of the catch per cope with the harsh conditions. The meadow spittlebug, sweep. Samples were taken between 09:00 and 16:30 Philaenus spumarius (L.) (Homoptera), is one of the most hours Sampling was performed only when vegetation common and ubiquitous insects in the meadows of the was dry to minimize differences resulting from the skerries (Halkka & Halkka, 1990). Extensive population vertical distribution of the insects. genetic studies indicate that dispersal between islands The relationship between spittlebug nymph survival, is extremely low (Halkka et al., 2001). This means that NAO and various climate variables was studied by the established populations are not significantly affected minicage method, which even provided an indepen- by migration. dent way to investigate effects of climate on spittlebug The meadow spittlebug has been found globally on abundance in 1969–1978. In the minicage method, the many thousands of food plant species and is certainly spittle mass with a P. spumarius nymph was enclosed one of the world’s most extreme polyphages. P. spumar- in a small round styrox box on the food plant. On the ius is a xylem feeder, and can ingest xylem sap 150–200 insides of the box halves, superlon rings were pressed times the body weight over 24 h (about 10 times the against the plant stem. The box was ventilated by nylon r 2006 The Authors Journal compilation r 2006 Blackwell Publishing Ltd, Global Change Biology, 12, 2250–2262 2252 A. HALKKA et al. windows. The spittlebug nymph emerged into adult the so-called extended winter (December–March) ver- in the box in about 2 weeks. The minicage method was sion of the index. used in the years 1969–1978 on the islands Allgrundet We tested for time lags between independent vari- and Porskobben. ables and population size with cross correlation func- Isolating nymphs in the very conspicuous spittle tion (CCF). Significant effects were found only for lag 0 masses was much more effective than collecting with except for population sizes which were autoregressive the sweep nets. Meadows were visited at least twice to at lag 1. Cross-correlations indicate spatial synchrony ascertain that practically all nymphs could be isolated among local populations. It has been known for a long in cages.
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