Swan foraging shapes spatial distribution of two submerged plants, favouring the preferred prey species

Compared to terrestrial environments, grazing intensity on belowground plant parts may be particularly strong in aquatic environments, which may have great effects on plant-community structure. We observed that the submerged macrophyte, Potamogeton pectinatus, which mainly reproduces with tubers, often grows at intermediate water depth and that P. perfoliatus, which mainly reproduces with rhizomes and turions, grows in either shallow or deep water. One mechanism behind this distributional pattern may be that swans prefer to feed on P. pectinatus tubers at intermediate water depths. We hypothesised that when swans feed on tubers in the sediment, P. perfoliatus rhizomes and turions may be damaged by the uprooting, whereas the small round tubers of P. pectinatus that escaped herbivory may be more tolerant to this bioturbation. In spring 2000, we transplanted P. perfoliatus rhizomes into a P. pectinatus stand and followed growth in plots protected and unprotected, respectively, from bird foraging. Although swan foraging reduced tuber biomass in unprotected plots, leading to lower P. pectinatus density in spring 2001, this species grew well both in protected and unprotected plots later that summer. In contrast, swan grazing had a dramatic negative effect on P. perfoliatus that persisted throughout the summer of 2001, with close to no plants in the unprotected plots and high densities in the protected plots. Our results demonstrate that herbivorous waterbirds may play a crucial role in the distribution and prevalence of specific plant species. Furthermore, since their grazing benefitted their preferred food source, the interaction between swans and P. pectinatus may be classified as ecologically mutualistic.
Introduction
Herbivores may have considerable impact on the distribution and population dynamics of plants (e.g. Maron and Crone 2006) as well as vegetation community structure (e.g. Augustine and McNaughton 1998), but non-grassland examples of such impacts are few. Similarities between aquatic and terrestrial systems and their dependence on top–down regulation are increasingly being appreciated by ecologists (Cyr and Pace 1993; Chase 2000). However, in these broad-scale inter-system comparisons, the predation of zooplankton on algae still plays a front-stage role in the representation of aquatic plant–animal interactions. The importance of vertebrate grazing on submerged macrophytes community structure remains disputed. Among the studies reported to date on interactions between aquatic herbivores and plants, few have considered the possibility of herbivory mediating competition between plants (but see Lauridsen et al. 1993; Van Donk and Otte 1996; Santamaría 2002; LaMontagne et al. 2003), and none have experimentally shown that this can lead to a specific herbivore-induced vegetation distribution and composition. Considering that the impact of herbivory on community structure in terrestrial systems increases with grazing intensity (Augustine and McNaughton 1998), the study of some aquatic plant–animal interactions with sometimes extremely high grazing pressures on both above- and belowground parts may prove rewarding.
Potamogeton pectinatus and P. perfoliatus are two species of aquatic macrophytes typical of eutrophic lakes, often co-occurring, with a more or less cosmopolitan distribution. They hibernate mainly vegetatively with rhizomes and turions (P. perfoliatus) or specialised tubers (P. pectinatus) in the sediment (Fig. 1). Many species of waterbirds rely on the leaves and seeds of these two species of water plants (Cramp and Simmons 1986). Among waterbird foragers, swans form a special group of consumers that are also capable of uprooting and consuming the belowground parts of P. pectinatus and P. perfoliatus. In particular, Bewick’s (Cygnus columbianus bewickii) and whooper swans (C. cygnus) are highly dependent on the nutrient-rich tubers of P. pectinatus (Nolet and Drent 1998; Nolet et al. 2001, 2002; Beekman et al. 2002).
Fig. 1Vegetative reproductive organs of Potamogeton perfoliatus and P. pectinatus. The tubers of P. pectinatus may considerably vary in size between approximately 2 and 16 mm. The depicted tuber is 15 mm long
The spatial distributions and segregation of P. pectinatus and P. perfoliatus have been studied extensively. Typically, P. pectinatus is found in shallower waters than P. perfoliatus. Lehmann et al. (1997) argued that the higher tolerance of P. pectinatus to wave exposure in shallow water and the higher tolerance of P. perfoliatus to light attenuation in deep water could be a major causal factor of this distribution of the two species. Scheffer et al. (1992) was able to explain about 50% of the variation in the distribution of both species by considering water depth, transparency, spring water temperature and exposure to waves for P. pectinatus and water depth and transparency for P. perfoliatus. During extensive studies on the distribution of aquatic vegetations and swan foraging in two of our major research sites where P. pectinatus and P. perfoliatus co-occur (Pechora Delta, in Arctic Russia, and Lake Ringsjön, in southern Sweden), we noticed that P. perfoliatus occurred not only in deep water but also in very shallow water seldom visited by tuber-feeding swans. We thus hypothesised that swan foraging, which is limited to areas of intermediate depth (Beekman et al. 1991; Nolet et al. 2001; Sandsten 2002), at least partly determines the distribution of P. perfoliatus.
In order to investigate how swan feeding on tubers of P. pectinatus affects the growth of P. perfoliatus, we monitored vegetation and swan foraging and performed a transplant experiment in Eastern Lake Ringsjön, Sweden. Potamogeton perfoliatus was planted in a P. pectinatus stand after which the development of both species was followed in the presence and absence of swan grazing.
Methods
Eastern Lake Ringsjön (55°52′N, 13°32′E) is a eutrophic, 20.5-km2 large lake with a maximum and mean depth of 16.4 and 6.1 m, respectively. The experiment was set up in Fulltofta Bay (0.7 km2, <1 m deep; Fig. 2), which is a wind exposed, shallow and sandy part of Eastern Lake Ringsjön, with an aquatic vegetation that nearly exclusively consists of P. pectinatus and P. perfoliatus. Every year from September to November, Fulltofta Bay hosts large numbers of migrating waterbirds (up to 1600 individuals, Sandsten 2002). Many of these migrating waterbird species, notably swans (whooper swans C. cygnus, Bewick’s swans C. columbianus bewickii, and mute swans C. olor), feed on tubers of P. pectinatus and rhizomes and turions of P. perfoliatus by digging in the sandy sediment (e.g. Cramp and Simmons 1986; Nolet and Drent 1998; Sandsten 2002). Coot (Fulica atra) and various species of ducks (mallard Anas platyrhynchos, pintail Anas acuta, wigeon Anas penelope, goldeneye Bucephala clangula, tufted duck Aythya fuligula, pochard Aythya ferina) may also forage on tubers, but nearly always in association with swans since they are unable to dig up the tubers from the sediment by themselves (e.g. Cramp and Simmons 1986; Sandsten 2002). Geese (mainly Anser anser) roost frequently in the area, but they very seldom feed on tubers (Cramp and Simmons 1986; personal observations, H. Sandsten).
Fig. 2Map of Lake Ringsjön with an enlargement of Fulltofta Bay and an overview of the bird-monitored and plant-monitored areas as well as the plant-experimental site. Enlargement of the plant-experimental site shows the six replicates of three treatments, with gray squares representing plots where no P. perfoliatus was planted and no protection from waterbirds was provided until 18 December 2000 at which time all treatments were covered with metal nets on the bottom (treatment p). Black squares represent plots with planted P. perfoliatus that were continuously protected by nets (treatment
). White squares represent plots with planted P. perfoliatus that were unprotected from 8 August to 18 December 2000 (treatment P)
To quantify our impression that P. perfoliatus occurs only in very shallow and relatively deep parts of Fulltofta Bay, we mapped the occurrence of P. pectinatus and P. perfoliatus in relation to water depth in Fulltofta Bay on 10 August 2000 (Fig. 2). Vegetation and water depths were examined on 173 points regularly spaced (at 20–30 m distance from point to point) in an area (0.12 km2) running from the shore to a depth of 1.2 m. The geographical position of each sampling point was measured with a GPS (Garmin Personal Navigator 12 XL). On each of the points we investigated plant occurrence three times by throwing a 50 × 50-cm metal frame into the water and diving down to look for plants. For P. pectinatus, a cover index was used, where 0 was no ramets m−2, 1 was 1–20 ramets m−2, 2 was 21–80 ramets m−2 and 3 was >80 ramets m−2. We counted all shoots emerging from the sediment surface as ramets. Potamogeton perfoliatus shoots were less frequent than P. pectinatus shoots and seldom found in the frames—possibly because of less favourable growing conditions but at least in part because of its morphology and growth strategy. We therefore used data on absence/presence in the proximity (within a radius of 10 m) of the sampling point. The data were entered into a geographic information system, GIS (Surfer 6.04) and interpolated over the entire monitored surface using intermediate distance interpolation.
Swans were counted over an area of 0.54 km2 from an observation point (Fig. 2) south of Fulltofta Bay on 5, 17 and 30 August, 10 and 23 September, 5, 18 and 28 October and 9 November 1999.
Swans foraging on tubers tread water to create a water current that flushes the sediment and uncovers tubers and rhizomes, resulting in the appearance of pits and piles of sediment on the bottom at the sites where foraging activity has taken place. Wave action will ultimately level the sediment again (Sandsten 2002). Depth heterogeneity was used as an indirect measure of waterbird foraging on tubers in the sediment. In order to investigate the timing of swan foraging in relation to water depth we measured depth heterogeneity along five fixed transects running parallel to the shore within the plant-monitored area. The transects were aimed to be at equidistant intervals parallel to the shore, but in fact they were located at a distance of 110, 180, 260, 340 and 400 m from the shore (mean depths were 37, 45, 60, 75 and 90 cm on 5 August 1999). Depth heterogeneity was obtained by calculating the SD from 5 × 10 measurements of water depth along each transect. Within every second metre along the 11-m-long transect ten water depths were measured at a distance of 10 cm, resulting in five SD from each transect. These five SD were entered as replicates from each transect in the statistical analysis and were also the basis for the graphical presentation of “mean standard deviation”. Measurements were conducted prior to and during the main swan grazing period on 5, 17 and 30 August, 10 and 23 September, 5 and 18 October and 1 and 12 November 1999. Depth heterogeneity in relation to time of measurement and mean water depth was statistically analysed using repeated measures ANOVA (Statistica ver. 5.1; StatSoft, Tulsa, OK). Normal distribution of residuals was checked with a probability plot, and heteroscedasticity of variances was checked for with Levene’s test. If the variances were not homogenous or the plots of residuals were not linear, the data were transformed to meet the assumptions of ANOVA.
The transplant experiment consisted of three separate treatments with six replicate plots (1.4 × 1.4 m), all situated in an established (at least for 5 years) stand of P. pectinatus in Fulltofta Bay (Fig. 2). The experiment ran from 31 May 2000 until 15 August 2001. One treatment,  consisted of continuously protected plots where rhizomes with ramets of P. perfoliatus had been planted among the P. pectinatus plants. The second treatment, P, consisted of plots where ramets of P. perfoliatus had also been planted among the P. pectinatus plants, but where swans were allowed to graze during the autumn migratory period (8 August until 18 December 2000). The last treatment, p, consisted of P. pectinatus plots without P. perfoliatus where swans were allowed to graze permanently. This last treatment was designed as a control treatment to check for any effects of the planting of P. perfoliatus on P. pectinatus. Ramets of P. perfoliatus were collected in the eastern part of the nearby Lake Krankesjön (55°42′N, 13°28′E) by scuba diving on 30 May 2000 just after onset of sprouting. The collected ramets with roots and intact meristems and varying in size from 30 to 70 cm were stored in plastic bags at 5°C overnight. On the following day, 22 ramets (density 11 m−2) with roots and intact meristems were planted in each of the  and P plots. The randomly selected ramets were distributed evenly over the plots and planted at a depth of 10 cm. The plots were subsequently protected with a 1.6-m high plastic net (mesh size 25 × 32 mm). The p plots were not protected since summer grazing on above- and belowground biomass of P. pectinatus is considered negligible (Santamaría 2002).
In all 18 plots, the above- and belowground biomass of the vegetation was surveyed by scuba diving and core sampling prior to the migratory and main grazing period of the swans, on 8 August 2000. After the main swan-grazing period (verified by counts on 18 July, 8 and 18 August, 8 September, 4 and 24 October and 2 November 2000, yielding 22, 18, 34, 10, 10, 10 and 10 swans km−2, respectively), the belowground biomass was again surveyed by core sampling on 18 December 2000. Finally, the effect of swan grazing  on the aboveground plant biomass during the autumn of 2000 was again assessed by scuba diving on 6 June and 15 August 2001 the following growth season. Aboveground biomass was evaluated by counting all ramets emerging from the sediment in two perpendicular transects (5 cm wide, 2.0 m long) running diagonally across each plot. Belowground biomass was sampled using four sediment core samples (diameter 11 cm, length 30 cm) in each plot. Roots, rhizomes and tubers of P. pectinatus and roots and rhizomes of P. perfoliatus were dried at 105°C for 24 h before dry weight (DW, g) measurements were taken. In December, we wanted to retain most of the P. pectinatus tubers for other purposes. Consequently, we first measured the fresh weight (FW, g) of each collected tuber and then assessed the DW on a subsample of randomly selected tubers. The regression of these DW estimates on FW was used to estimate total tuber DW of the whole sample (DW = 0.2953 FW, P < 0.0001, R2 = 0.958, n = 33).
Lake Ringsjön is usually covered with ice during the winter, which poses a potential threat to the fences around the plots. Therefore, on 18 December 2000, when the majority of birds had left the bay, the fences of treatment  were removed. Subsequently all plots, of treatments P and p, were covered with metal nets (mesh width 10 × 10 cm) to protect them from belowground winter grazing by swans during occasional periods when the lake was not ice-covered. These bottom-covering nets remained in place throughout the experiment, and counting of ramets in 2001 was carried out without removing the nets.
The experimental data were analysed with analysis of variance, ANOVA, in Statistica ver. 5.1. Heteroscedasticity and residuals were examined, and transformations were carried out using the same methods as for the depth heterogeneity data. Tukey’s honestly significant difference (HSD) was used to test all pairwise comparisons among means when the overall treatment effect in the ANOVA was (near) significance.
Results
Vegetation and water depth mapping
The shallowest (<20 cm) and deepest (>95 cm) parts of Fulltofta Bay were void of submerged macrophytes (Fig. 3). Potamogeton pectinatus grew at depths varying from 20 to 95 cm, with the highest ramet densities at intermediate water depths. In contrast, P. perfoliatus was found at relatively few points and mainly in deep water (>70 cm). Some P. perfoliatus was also found in shallow water (20–30 cm) but except for one finding at a depth of 46 cm, no P. perfoliatus was found at intermediate water depths (30–70 cm).Fig. 3Maps on vegetation and water depth in Fulltofta Bay, Lake Ringsjön. The vertical line shows the same point in the three maps. The upper map shows the distribution of P. perfoliatus on deep and shallow water. Grey represents areas where the probability of encountering P. perfoliatus on the sampling points was larger than 50%. The middle map shows the distribution and abundance of P. pectinatus. The lower map is a three-dimensional presentation of water depths in the monitored area
Swans
Figure 4 (upper panel) shows swan densities in Fulltofta Bay during the autumn of 1999; swan grazing followed a similar temporal pattern in 2000 (Sandsten 2002). Depth heterogeneity largely coincided with swan densities and increased with time, indicating that swan grazing on P. pectinatus tubers increased from August to early November (Fig. 4, lower panel). Depth heterogeneity was significantly affected by time and the interaction between water depth and time [F8,160 = 14.38 P < 0.001, F32,160 = 3.65 P < 0.001, F4,20 = 1.80 P = 0.168; respectively; data was ln (Y + 0.1) transformed]. The interaction between time and water depth indicates that over time the swans’ main foraging depth changed. As shown in Fig. 4, birds started foraging on macrophytes at shallow depths (37 and 45 cm) in August, shifting to deeper areas (60, 75 and 90 cm) in October and November. During the last days of October, stormy weather events evened out the sediment, resulting in little depth heterogeneity being recorded on 1 November.Fig. 4The upper panel shows swan densities in Fulltofta Bay (area 0.54 km2) over the period August–November 1999. Swans include the whooper swan (Cygnus cygnus), Bewick’s swan (C. columbianus bewickii) and mute swan (C. olor) The lower panel shows water depth heterogeneity measured as 5 SD of water depth at five locations with different water depths. The columns show mean + standard error of these SD. Depth heterogeneity is used as an indirect measure of swan foraging on tubers in the sediment
Transplant experiment
During the summer following planting, P. perfoliatus established well in the  and P plots, as indicated by the August 2000 sampling (Fig. 5) prior to the peak swan-grazing period (compare Fig. 4). A comparison of the  and P treatments revealed that neither belowground biomass nor ramet density of P. perfoliatus differed significantly at the start of the experiment (Table 1; Fig. 5). As expected, no P. perfoliatus was found in the p plots where no P. perfoliatus had been planted.Fig. 5Above- and belowground biomass (means and standard errors) of P. pectinatus and P. perfoliatus in the transplant experiment during various times of the year in 2000 and 2001.  six plots where P. perfoliatus was planted in May 2000 and where above- and belowground biomass was protected against waterbird herbivory until December 2000, P six plots where P. perfoliatus was planted in May 2000 and above- and belowground biomass was protected against waterbird herbivory until August 2000, p six “unplanted” plots without protection against herbivores until December 2000. All 18 plots were protected from waterbirds after December 2000 with metal nets covering the bottomTable 1ANOVA table for above- and belowground data of Potamogeton perfoliatus and P. pectinatus sampled in the three treatments on 8 August 2000 before the peak of waterbird herbivorySource of variationPotamogeton sp.FdfPRamets (number m−2)P. pectinatusa0.621,10NSP. perfoliatus a1.61,10NSP. pectinatus b1.02,15NSBelow-ground DW (g m−2)P. pectinatusa0.861,10NSP. perfoliatusa2.21,10NSP. pectinatusb3.32,15NS (0.065)*Tubers (number m−2)P. pectinatusa3.01,10NSP. pectinatusb1.72,15NS*Tukey’s HSD multiple comparison between treatments resulted in a near significant effect (P = 0.058) for the comparison between  and p; NS, not significantaPlots without planted P. perfoliatus excludedbAll plots included
The August sampling also showed a healthy stand of P. pectinatus in all plots before the peak swan-grazing period. Although there seemed to be a tendency for P. pectinatus to perform worse in the presence of P. perfoliatus, no significant differences in belowground DW, ramet density or P. pectinatus tuber density were detected between the treatments (Table 1; Fig. 5).
In December, when the majority of swans had left the lake, belowground DW was again estimated (Fig. 5). Potamogeton perfoliatus was found in three of the  and none of the other plots. Although this result suggested a negative impact of swan grazing on P. perfoliatus, it did not allow for any meaningful statistical analysis. In December, P. pectinatus belowground biomass and tuber density were higher in the  plots than in the P plots [F1,10 = 7.7, P < 0.05 after ln(Y + 1) transformation, and F1,10 = 12, P < 0.001 after square root (Y + 1) transformation, respectively], revealing the effect of tuber consumption by swans.
Ramet densities in the plots were counted in June 2001. There were significant treatment effects both on P. pectinatus and P. perfoliatus, and both species were present at higher densities in the  plots than in the P plots (Fig. 5; Table 2). In August 2001 there was still a difference in P. perfoliatus ramet density but not in P. pectinatus (Fig. 5; Table 2).Table 2ANOVA table on P. pectinatus and P. perfoliatus ramet density in P and  plots on 6 June and 15 August 2001Source of variationPotamogeton sp.FdfPRamets (n m−2) in JuneP. pectinatus431,10***Ramets (n m−2) in JuneP. perfoliatus5651,10***Ramets (n m−2) in AugustP. pectinatus1.11,10NSRamets (n m−2) in AugustP. perfoliatus451,10******P < 0.001; NS, not significantAll data is ln(Y + 1) transformed
Discussion
Our vegetation mapping study supports our earlier impression that the distribution of P. perfoliatus is limited to those areas where the pressure of swan grazing is low. It also shows that P. pectinatus grows at intermediate water depths, while P. perfoliatus is found mainly in deep water and occasionally at shallow depths. This is consistent with reports in the literature that P. perfoliatus mainly grows deeper than P. pectinatus (Scheffer et al. 1992; Lehmann et al. 1997), although we found no other report on P. perfoliatus growing in very shallow water.
Depth heterogeneity substantiated our impressions of the spatial variation in foraging activity of the swans in Fulltofta Bay. Swans showed a tendency to forage at intermediate depths that are largely void of P. perfoliatus. They started to forage in relatively shallow water and moved to deeper parts, where foraging is more expensive (Nolet et al. 2001), later in the season. A similar phenomenon was observed in Bewick’s Swans foraging on P. pectinatus in the Russian White Sea (Nolet and Drent 1998). This shift into deeper water over time may not only have been a consequence of depletion—it may also have been related to a decrease in the water table by 0.2 m from August to early November (Swedish Meteorological and Hydrological Institute, unpublished data). When the spatial variation in foraging activity was considered over the whole season, there was a tendency for intermediate water levels to be used more frequently than the shallow and deep parts of the bay. This result is in accordance with those from an experiment on tuber depletion at different water depths in Fulltofta Bay (Sandsten 2002) and with previous observations on P. pectinatus foraging swans elsewhere (Beekman et al. 1991; Nolet et al. 2001). The observed tendency of swans to preferentially forage at intermediate depths becomes even more striking when we study the depth heterogeneity in Fulltofta Bay during the month of October 1999, when swan numbers were peaking.
The results of the transplant experiment showed that subterranean swan grazing had a dramatic negative effect on P. perfoliatus and, consequently, on the spatial depth-related distribution of P. pectinatus and P. perfoliatus in Fulltofta Bay and possibly elsewhere. When faced with increased subterranean herbivory, P. pectinatus seems to increase the depth at which its tubers are buried—likely as a defence mechanism to reduce tuber loss (Klaassen and Nolet 2007; Santamaría and Rodríguez-Gironés 2002). However, during the August–December 2000 period, P. pectinatus winter biomass was considerably reduced as a result of swan foraging. Both belowground tuber biomass and tuber numbers were negatively affected. At the same time, swan foraging also had a marked negative effect on the occurrence of P. perfoliatus in the following year. Potamogeton perfoliatus had virtually disappeared from the unprotected sites where waterbirds had free access: in December, directly after herbivory, no belowground remnants of P. perfoliatus were detected; in June and August of the following year, the aboveground presence of P. perfoliatus was marginal in the unprotected plots, which contrasted sharply with the situation in the plots that had been continuously protected from subterranean herbivory by swans. Although not as dramatic as in P. perfoliatus, tuber herbivory by swans also had an effect on the aboveground biomass of P. pectinatus in the spring, but differences in aboveground biomass between protected and unprotected plots were no longer detectable by August 2001. The small number of tubers remaining in P was probably sufficient to produce a large number of tubers during the following autumn. This result is consistent with observations by LaMontagne et al. (2003) and the model of Jonzén et al. (2002), which suggest that tuber herbivory in winter leads to a lower density of ramets the following spring, but that compensation (or even overcompensation; compare Nolet 2004) of tuber production may occur the following autumn.
In Sweden, the investments of P. perfoliatus and P. pectinatus in vegetative reproduction are large. It is highly likely that the difference in their wintering strategy determines their susceptibility to subterranean foraging by swans and, consequently, their prevalence in sites regularly frequented by digging swans. The small, round and relatively robust tubers of P. pectinatus are a highly preferred food source by foraging swans (e.g. Cramp and Simmons 1986; Sandsten 2002; Nolet and Drent 1998). However, if missed and not eaten, they are very likely to survive the digging and uprooting activity of the swans. In contrast, the rhizomes and turions of P. perfoliatus are long, interconnected and relatively fragile. Compared to the solitary tubers of P. pectinatus, they are easily detected and, if not eaten, fragmented by the digging and uprooting of swans.
The experiment reported here was mainly designed to study competition between P. pectinatus and P. perfoliatus under autumnal swan grazing. However, during the early experimental phase, which was without grazing until August 2000, no effect of P. perfoliatus on P. pectinatus growth was observed. Nevertheless, it is rather conceivable that both species compete for nutrients and light and that the removal of P. perfoliatus by swans will ultimately be of benefit to P. pectinatus. Therefore, the swans ultimately increase the profitability of the vegetation to themselves by promoting the nutrient-rich tuber-producing P. pectinatus. Although subterranean feeding in P. pectinatus stands may also favour the establishment of new macrophyte species (LaMontagne et al. 2003), the current findings suggest that tuber-feeding herbivores may actually stimulate the development of P. pectinatus by mediating competition with other macrophyte species, notably P. perfoliatus. This outcome implies a potentially mutualistic relationship, at least in an ecological sense (sensu Järemo et al. 1999), between a predator (swan) and its prey (P. pectinatus). Following Järemo et al.'s (1999) classification of mutualistic plant–herbivore interactions, the current relationship may represent a “plant–herbivore antagonism”, where P. pectinatus has adapted itself better than competing plants to subterranean herbivory (by producing specialised clonal propagules and hiding; Klaassen and Nolet 2007) thus obtaining a relative fitness advantage over less well-adapted species such as P. perfoliatus. However, since overcompensation to subterranean grazing may occur (Santamaría and Rodríguez-Gironés 2002; Nolet 2004), the relationship between P. pectinatus and swans may also be considered as an “evolution of overcompensation relationship”, in which P. pectinatus has an absolute fitness advantage to grazing, whereas its competitors have not.
Our data support the view that waterbirds may play a crucial role in the prevalence of certain plant species with potential consequences for the functioning of the system as a whole (e.g. Engelhardt and Ritchie 2001). Reviewing the (terrestrially-skewed) literature, Augustine and McNaughton (1998) concluded that the impact on vegetation communities tends to increase with grazing intensity. In aquatic systems, belowground grazing may be facilitated by the generally softer and easily penetrable sediments, notably if grazers make use of water jets to uncover the vegetative plant parts. Grazing intensity may thus reach very high levels in these systems, resulting in very rapid alterations in vegetation composition that are uncommon in terrestrial systems.

potamogeton
cygnus
subterranean herbivory
mutualism
predator–prey interactions


Osteoma in the upper cervical spine with spinal cord compression

Osteoma is a common benign tumor. It occurs dominantly at the skull bone. Outside skull osteoma is rare, and primary intra-canal osteoma is extremely rare. To the author’s knowledge, only 14 cases of osteomas of the spine had been reported, in which only seven cases were in English literature. The authors reported two rare cases of intra-canal osteoma of the upper cervical spine with cord compression. Included are pertinent history, physical examination, rontgenographic evaluation before and after operation, surgical interventions, pathological study, and outcome. The available literature is also reviewed. On systemic examination and rontgenographic study, these two cases were found to have bone tumor in the upper cervical canal. Surgical interventions were performed, one with an en bloc excision, the other with a subtotal excision. The pathological study demonstrated a diagnosis of osteoma. After a follow-up with 20 and 15 months, the clinical symptoms of both cases significantly improved.
Introduction
Osteomas are rare, slow growing lesions composed of compact bone that occur almost exclusively in the skull [2, 7], most often in the inner and outer table of the calvarium or in the bones of the face or mandible [1, 12, 13]. The prevalence of this disease amounting those who have had sinus radiographs has been estimated to be 0.42% [7]. Although these lesions may cause sinusitis or exophthalmos when they arise from the wall of the nasal sinuses or the orbit, cranial osteomas often cause no symptoms and are discovered incidentally.
Primary intra-canal osteomas are extremely rare. To the authors’ knowledge, at the time of writing, only 14 cases of osteomas of the spine had been reported, in which only seven cases were in the English literature [4–6, 8, 9, 11].
The purpose of this article is to report on two patients who presented with cervical intra-canal osteoma.
Case report
Case One
A 56-year-old man had presented with paresis and weakness of his extremities after a hyperextension injury of the cervical spine in August 2002. The man had been asymptomatic prior to the accident.
Physical examination demonstrated limitation in neck rotation, and motor weakness of the extremities with strength 3/5 in upper extremities and 4/5 in lower extremities. He could eat with chopsticks to a limited degree. He could walk. However, he needed cane or aid on stairs. Hypoesthesia was present at the upper extremities, bilaterally. The biceps tendon reflex, patellar tendon reflex, and Achilles tendon reflex were hyperactive, and the Hoffman and Babinski reflex were positive bilaterally. Sustained ankle clonus was present, bilaterally. Neurological examination was consistent with upper neuron cell injury. The Japanese orthopedic association (JOA) score for cervical myelopathy was 11.
Preoperative imaging study demonstrated a cortical like solid lesion. The results were shown in Fig. 1a–e.
Fig. 1a Cervical A–P view X-ray showed densification at left side at C2–3 level. b Cervical lateral view X-ray showed high density at C2–3 level, the facet joints between C2\C3 were obscure. c CT scan through the intervertebral foramen between C2 and C3 showed the tumor occupied more than 60% canal and the vertebral shape changed, caused by the chronic pressure. d Three dimensions CT reconstruction showed the three-dimension relationship between the tumor and the cervical spinal canal. e Middle sagittal plane T1WI MRI showed the spinal cord was pressed by the tumor. The signal of the tumor was low. f The same plane as c after operation, showed the whole decompression of the spinal canal, part of the tumor, near the vertebral artery was left. g The same plane as e after operation, showed the whole decompression of the cord and spinal canal. h, i The pathological study showed that the lesion was composed of uniformly dense, compact, cortical-like mature lamellar bone. H: ×100, I: ×400
We performed a leminectomy of C2 and C3. In the operation, we found that the tumor was adhesive with the left side vertebral artery. To avoid the injury of the artery, part of the tumor, near the vertebral artery, was left. However the decompression of the spinal cord was enough (Fig. 1f–g). The pathological study showed that the lesion was composed of uniformly dense, compact, cortical-like, mature lamellar bone (Fig. 1h–i), and a diagnosis of osteoma was made. Two weeks after the operation, this patient’s clinical symptoms improved significantly. Then, with hard cervical brace protection, the patient was permitted to ambulate. He noted gradual improvement of strength in his upper extremity. Three months later, the brace was removed. Twenty months later, the muscle strength was 5/5 in all extremities. He could eat with chopsticks, but awkwardly. He could walk with no disability. No hypoesthesia was present. The patient’s JOA score increased from 11 to 16 (Table 1).
Table 1JOA score of the two cases before and after therapyBefore therapyFollow-upCase 1Case 2Case 1Case 2Motor Upper extremity2133 Lower extremity2243Feeling Upper extremity1122 Trunk2222 Lower extremity2222Sphincter2233Total11101615
Case two
A 49-year-old man had experienced paresis and weakness of his extremities after a weight-hit injury of the head in November 2002. The man had been asymptomatic before the accident. Physical examination showed moderate motor weakness and hypoesthesia of the upper extremity, with strength 3/5 in upper extremities and 4/5 in lower extremities. He could eat with spoon but could not with chopsticks. He could walk. However, he needed a cane or aid on stairs. The feel of trunk and lower extremity is fair. The biceps, patellar, and Achilles tendon reflexes were hyperactive, and the Hoffman and Babinski reflexes were positive bilaterally. Ankle clonus was noted continuously on both sides.
Preoperative imaging study demonstrated lamina fracture of C3, traumatic instability of C3–5, and a cortical like solid lesion at the left side of C2 lamina. The results were shown in Fig. 2a–c.
Fig. 2a Cervical lateral view X-ray showed high density at C2–3 level, the facet joints between C2\C3 were obscure, traumatic instability of C3–5. b CT scan through C2 showed the tumor at the left side of the lamina, occupied about 20% canal, and the left side lamina of the C2 became thicker. c Sagittal plane T2WI MRI showed the spinal cord was pressed by the tumor. The signal of the tumor was low. d Three-dimension CT reconstructive image showed complete decompression
We performed a laminectomy of C3–C4 and part of C2, as well as internal fixation of C3–5, using pedicle screw system. The tumor was removed completely and the spinal cord was decompressed. The pathological study showed that the lesion was also composed of uniformly dense, compact, cortical-like, mature lamellar bone without nidus (not shown). Lateral view X-ray after operation showed the reconstruction of the stability by the pedicle screw system and lamina decompression of C3–4 and part of C2. Three dimension CT reconstructive image showed complete decompression of the spinal cord (Fig. 2d).
A month after the operation, this patient’s clinical symptoms improved significantly. Then, with hard cervical brace protection, the patient was permitted to ambulate, and he noted gradual improvement of strength in his upper extremity also. Three months later, the brace was removed. After 15 months, the muscle strength was 4/5 in upper extremity and 5/5 in lower extremity. He could eat with chopsticks, but awkwardly. He could walk without cane or aid, but slowly. No hypoesthesia was present. The JOA score increased from 10 to 15 (Table 1).
Discussion
Congenital disease, rheumatoid arthritis, fracture and dislocation, and other systemic diseases can cause the compression of the upper cervical spinal cord [14]. However, osteoma is one of the rare reasons. Osteoma is defined by WHO as a benign lesion consisting of well differentiated mature bone tissue with a predominantly laminar structure, and showing very slow growth. Osteomas are bosselated, round to oval sessile tumors that project from the subperiosteal or endosteal surfaces of the cortex [3]. They are composed of a composite of woven and lamellar bone that is frequently deposited in a cortical pattern with haversian-like systems. Some variants contain a component of trabecular bone in which the intertrabecular spaces are filled with hematopoietic marrow [10]. Osteoma usually occurs in the skull. Only occasionally have these lesions been reported in extracranial locations (Table 2). In 1980, Pecker et al. reported the first osteoma in cervical inter-vertebral foramen. They used a Lateral interscalenic approach to excise the lesion [8]. In 1986, Lantsman reported six cases of osteoma in spine, but the article was in Russian, no more details could be reviewed [4]. In 1993 [5] and 1996 [6] Laus reported the same case in Italian and English. To excise the lesion, they performed an anterior prevascular extra oral approach. In 1996 [9], Peyser reported 11 cases of extracranial osteoma, in which five were in spine, one in the cervical spine, two in the lumbar spine and two in the scrum spine. In 1998 [11], Rengachary reported that another osteoma affected the cervical spine.
Table 2Cases reported in the literatureReferencesArticle languageCase numberSite of the lesionRecurredRengachary [11]English1CervicalNoPeyser [9]English5Cervical (1), lumbar (2), sacrum (2)One pain recurredLaus [6]English1CervicalNoLaus [5]Italy1CervicalNoLantsman [4]Russian6SpineNoPecker [8]French1CervicalNoTotal14aaLaus M. reported the same case in English and Italy
The diagnosis of intra-canal osteoma is still confusing. In Peyser’s series [9], none of the cases had correct diagnosis before the operation. In our cases, the rontgenographic study before operation could give some clues, but the final diagnosis still depended on the pathological findings. Histologically, the reactive bone induced by infection and trauma may be similar with a true osteoma [10]. However the differential diagnosis can be made by the tumor’s site and pertinent history. Traumatic reactive bones are most frequently observed in relation to the femur, beneath the quadriceps, in relation to the adductor magnus (the so-called rider’s bone) or in relation to the medial collateral ligament of the knee joint. The condition is also not infrequent at the elbow, the exostosis forming in the intermuscular planes of the brachialis following dislocation. Injury leads to the formation of a subperiosteal hemorrhage, the periosteum being detached by muscular traction. If the periosteum remains intact, the hematoma may become absorbed; but if the periosteal reapposition and the absorption of the blood clot are prevented, traumatic bone overgrowth may occur. However, this condition could not occur at the endosteum. In the case of infective reactive bones, an infection history of relevant site should be noted.
The clinical features of osteoma in the spine may be confusing. Cranial osteomas often cause no symptoms and are discovered incidentally, although these lesions may cause sinusitis or exophthalmus when they arise from the wall of the nasal sinuses or the orbit. It would be expected that the symptoms of spinal osteoma would depend on the location of the lesion and its relationship with the peripheral tissue. As Rengachary [11] and Laus [5, 6] reported, the symptom of the spinal osteoma was caused from spinal cord or nerve root pressure. However in Peyser’s series all but one of the patients was symptomatic and had dull, aching pain at the time of the initial presentation. In our series, the two cases had no symptom before the injuries. It may be because osteomas are benign and very slow-growing lesions. And the spinal cord and never roots may adapt to the chronic pressure. Since the lesions cause spinal canal stenosis, they can cause the spinal cord to be more easily damaged by minor injury.
The growth potential of osteoma remains unclear, as we know the cranial osteomas grow very slowly. Peyser’s excellent work showed us the growth potential feature of the spinal osteoma [9]. In their series, one patient who had a juxtacortical osteoma of the cervical spine, showed no major change on serial CT scans performed twelve years apart. However, another patient’s sacral osteoma showed significant growth on serial radiographs performed 18 years apart. The method of surgical management of an osteoma depends on the growth feature of the tumor. Cranial osteoma does not need surgical excision if there are no symptoms. The aim of surgical management of spinal osteoma is decompression and stabilization if instability exists. Rengachary and Laus performed total excision of the lesion, with no tumor recurrences. Peyser performed three total and two subtotal excisions, in the case series of osteomas, none recurred. However in one of the patients, partial resection of an osteoma from the body of the fifth lumbar vertebra resulted in no relief of pain and necessitated an additional procedure to remove the remainder of the lesion. In our series, it was relatively easy to perform an en bloc excision in the second case. In the first case, in view of a patient’s age and risk of vertebral artery injuries, a subtotal excision was performed, also with satisfied short time outcome. However, the follow-up was not long enough to observe the recurrence.
Conclusion
The incidence of intra-canal osteomas is rare. It can cause upper cervical myeolopathy. The rontgenographic study before operation can give some clues, but the final diagnosis still depends on the pathological findings. Surgical treatment, either en bloc or subtotal excision of the lesion, may be effective.

osteoma
cervical spine
intra-canal
myeolopathy
operative treatment


Homotypic Versus Heterotypic Continuity of Anxiety Symptoms in Young Adolescents: Evidence for Distinctions Between DSM-IV Subtypes

Objective: to investigate homotypic and heterotypic longitudinal patterns of symptoms of separation anxiety disorder (SAD), generalized anxiety disorder (GAD), social phobia (SoPh), panic disorder (PD), and obsessive compulsive disorder (OCD) in young adolescents from the Dutch general population.
Introduction
Anxiety disorders are among the most prevalent psychiatric disorders in children and adolescents (Costello et al., 1996; Essau et al., 2000; Verhulst et al., 1997), are persistent, and are associated with impaired functioning (Canino et al., 2004; Ferdinand & Verhulst, 1995; Ferdinand et al., 1995; McGee & Stanton, 1990; Pine et al., 1998; Verhulst et al., 1997). The high degree of comorbidity amongst anxiety disorders in children and adolescents seems to point in the direction of one taxonomic construct, instead of a number of separate disorders. High comorbidity rates have been reported by many authors (Essau et al., 2000; Masi et al., 1999; Newman et al., 1996; Verduin & Kendall, 2003). Evidence for a higher order factor that explains the presence of different types of anxiety has been found in children (Nauta et al., 2004) and adults (Hettema et al., 2005; Krueger, 1999; Vollebergh et al., 2001). Negative affectivity (NA) (Chorpita, 2002; Clark, 2005; Clark & Watson, 1991; Lonigan et al., 1999, 2003) may be one of the higher order factors that may explain the finding of heterotypic continuity. NA represents displeasurable engagement with the environment and a sense of high subjective distress (Lonigan et al., 2003), and is often considered as a temperament trait that is associated not only with anxiety, but with depression as well (Clark, 2005).
Using data collected at the first assessment wave of a study that was also used to conduct the research that is being described in the present manuscript, support was found for the presence of one single anxiety dimension, instead of a number of separate anxiety concepts (Ferdinand et al., 2006). The sample of this previous study consisted of 10- to 12-year-olds from the Dutch general population, who completed a self-report questionnaire for anxiety symptoms. Based on item scores on this questionnaire, latent class analysis did not detect classes of individuals with, for instance, high scores on items tapping separation anxiety, and simultaneously low scores on items tapping panic or social anxiety. Instead, high scores on one anxiety dimension implicated high scores on the other anxiety dimensions as well. However, other studies found evidence for separate anxiety dimensions. By performing factor-analyses, several authors found that DSM-IV anxiety disorders, such as generalized anxiety disorder, separation anxiety disorder, social phobia, and panic disorder represent different problem dimensions in children and adolescents (Chorpita & Daleiden, 2000; Muris et al., 2002; Spence, 1997).
Longitudinal studies can provide valuable information regarding taxonomic constructs. For instance, it was found that symptoms of social phobia in adolescents predicted similar symptoms in adulthood (Pine et al., 1998). The prediction of a disorder by the same disorder is called homotypic continuity. However, social phobia symptoms also predicted simple phobia in adulthood. The prediction of a disorder by another disorder is called heterotypic continuity (Costello et al., 2003). Several mechanisms may explain heterotypic continuity. Heterotypic continuity may occur by chance. In other words, disease A may disappear, and disease B may occur subsequently, as a coincidence. However, in that case, continuity would not be reflected in statistical significance. More likely reasons for heterotypic continuity would be that disease A would be the cause of disease B, or that disease A and B share a common vulnerability factor.
The aim of the present study was to investigate homotypic and heterotypic longitudinal patterns of symptoms of separation anxiety disorder, generalized anxiety disorder, social phobia, panic disorder, and obsessive compulsive disorder in young adolescents from the Dutch general population. For this purpose, individuals from a community sample, who were assessed for the first time when they were aged 10 to 12 years, were followed up across a period of two years. At both assessments, anxiety symptoms were assessed with a self-report questionnaire. Given mixed results of previous studies, we did not formulate specific hypotheses regarding the level of homotypic or heterotypic continuity of different types of anxiety.
Methods
Sample and procedure
The TRacking Adolescents’ Individual Lives Survey (TRAILS) is a prospective cohort study of Dutch early adolescents aged 10–12 years, who are followed biennially. The present study used data from the first (2001–2002) and second (2003–2004) assessment wave. The TRAILS target sample consisted of young adolescents from five municipalities in the North of the Netherlands, including both urban and rural areas. More details about the sample selection have been published elsewhere (de Winter et al., 2005).
Of all subjects who were approached at wave 1 (N = 3,145), 6.7% were excluded. The exclusion criteria were (1) adolescent incapable to participate because of mental retardation or a serious physical illness or handicap and (2) Dutch-speaking parent or parent surrogate not available, and not feasible to administer a part of the measurements in parent’s own language. Of the remaining 2,935 young adolescents, 24% did not want to cooperate, and 76.0% cooperated with the study at wave 1 (N = 2,230, mean age 11.09 years, SD .55, with 50.8% girls). Most frequent reasons for non-response were ‘not interested’ (33.8%), participation in other research or unfavorable experiences with research (15.4%), too much of a burden on the child (12.2%), lack of time (10.3%), concerns about privacy and confidentiality (8.0%), and the child’s refusal to participate because friend(s) did not participate (4.0%). In 34 cases (1.2%) we failed to contact anyone of the household (de Winter et al., 2005). Responders and non-responders did not differ with respect to the proportion of single parent families, or the prevalence of teacher-rated problem behavior. Furthermore, no differences between responders and non-responders were found regarding associations between socio-demographic variables and mental health outcomes (de Winter et al., 2005). To assess anxiety symptoms, the Revised Child Anxiety and Depression Scale (RCADS) (Chorpita & Daleiden, 2000) was used at wave 1, and also at wave 2. For 20 cases, RCADS data were not obtained at wave 1 because respondents were not present during the measurements that were conducted in the classrooms, and could not be reached afterwards. Hence, RCADS data of 2,210 pre-adolescents were available at wave 1.
At the second assessment wave, following similar procedures as at wave 1, RCADS information was obtained from 2,067 individuals. This was 95.5% of those for whom wave 1 RCADS information had been collected (51.4% girls). To examine possible selective attrition, a stepwise logistic regression analysis was performed with ‘wave 2 RCADS information available’ as a dependent variable, and wave 1 age, sex, and the wave 1 RCADS Total Anxiety score (that was constituted by summing scores on the five anxiety dimensions that were assessed with the RCADS in the present study, see below) as possible predictors. The RCADS Total Anxiety score and sex did not predict attrition. However, younger age predicted attrition significantly (odds ratio = .17, Wald = 93.1, p < .001; Model chi-square = 109,551, df = 1, p < .001). Cox and Snell R-square of the regression model was .048, which indicated that the effect of age was small. Further, most importantly, the level of anxiety at the initial assessment did not influence cooperation at wave 2.Table 1RCADS itemsSADSoPhFears being alone at homeWorried when does poorly at thingsScared to sleep aloneWorried when somebody angryScared to sleep away from homeWorried will do badly at schoolFears being away from parentsWorried about mistakesWorried in bed at nightWorried what others thinkTrouble going to schoolScared to take a testAfraid of being in crowded placesWorried might look foolishAfraid to talk in front of classAfraid to look foolish in front of peopleGADPDWorried something awful will happen to familySuddenly trouble breathing without reasonWorried bad things will happen to selfWhen has a problem, feels shakyWorried something bad will happen to selfSuddenly trembling, shaking without reasonThinks about deathSuddenly dizzy, faint without reasonWorried about thingsWhen has a problem, stomach feels funnyWorried about what will happenWhen has a problem, heart beats really fastSuddenly feeling scared without reasonSuddenly heart beats too fast without reasonWorried suddenly get scared without reasonOCDCan’t get silly/bad thoughts out of headKeeps checkingHas to think thoughts to stop bad eventsHas to do things over and over againHas to do things just right to stop bad eventsBothered by bad/silly thoughts or images
Measures
The Revised Child Anxiety and Depression Scale (RCADS) (Chorpita & Daleiden, 2000) is a revision of the Spence Children’s Anxiety Scale (SCAS) (Spence, 1997). It is a self-report questionnaire with 47 items, that are scored on a 4-point scale (0 = never, 1 = sometimes, 2 = often, 3 = always). The questionnaire covers six scales, corresponding with DSM-IV dimensions of anxiety disorders and depressive disorder. The following five scales were used for the present study: separation anxiety disorder (SAD), generalized anxiety disorder (GAD), social phobia (SoPh), panic disorder (PD), and obsessive compulsive disorder (OCD) (see Table 1). The scale major depressive disorder (MDD) was not used. The internal consistencies of the scales that were used were (respectively at wave 1/wave 2) .66/.59 for SAD, .80/.72 for GAD, .78/.88 for SoPh, .75/.72 for PD, and .68/.66 for OCD. The factor structure—for all six scales together—that was originally based on data from 1,641 children and adolescents from a community sample from Hawaii (Chorpita & Daleiden, 2000), was confirmed by confirmatory factor analysis in the TRAILS sample at wave 1 (fit indices of NNFI = .96, RMSEA = .05, and SRMR = .05, indicating an adequate fit to the sample data) (Ferdinand et al., 2006). The association of RCADS dimensions of anxiety with corresponding DSM-IV anxiety disorders was supported by previous research (Nauta et al., 2004).
Statistical analyses
First, to obtain information regarding comorbidity between different types of anxiety problems in the study sample, correlations among wave 1 RCADS scale scores were computed for each sex. Then, Pearson correlations were computed between wave 1 and wave 2 RCADS scale scores, separately for each sex group. Correlations provide insight in the associations between measures. However, by just computing correlations, it can not be judged if continuity is homotypic or heterotypic. For instance, the magnitude of a correlation between wave 1 SAD and wave 2 SoPh scores depends on the correlation between wave 1 SAD and wave 1 SoPh scores. The higher correlations between wave 1 SAD and wave 1 SoPh are, the higher the correlation between wave 1 SAD and wave 2 SoPh will be. In other words, if assessment of continuity would solely be based on correlations, comorbidity at wave 1 would artificially inflate estimations of the extent of heterotypic continuity between wave 1 and wave 2.
To correct for the effects of wave 1 comorbidity rates, regression analyses were conducted. First, it was assessed which part of continuity in anxiety problems was typically homotypic. For this purpose, for scores on each of the five RCADS scales at wave 2, a set of regression analyses was conducted, with wave 2 RCADS SAD, GAD, SoPh, PD, and OCD scores as dependent variables. These analyses were conducted to investigate how much of the variance in a specific RCADS scale score at wave 2 was not accounted for by an overall elevation in different types of anxiety at wave 1, but instead, specifically by its own counterpart at wave 1. We will now describe the regression analyses that were conducted for wave 2 SAD. Those for GAD, SoPh, PD, and OCD were similar. In the first block of the analyses, wave 1 scores on GAD, SoPh, PD, and OCD were entered simultaneously as predictors. Then, in a second block, wave 1 scores on the SAD scales were added, to see how much of the variance in wave 2 scores was predicted specifically by wave 1 SAD scores, and not by scores on the other RCADS scales at wave 1. This variance reflects specific homotypic continuity. In the third block, sex was added. In the fourth block, an interaction between sex and SAD was added. If this interaction was significant, analyses were conducted for girls and boys separately. For each next block, the variance that was accounted for by the variable in this block was computed (R2).
Second, it was assessed which part of continuity in anxiety problems was specifically heterotypic. For this purpose, for scores on each of the five RCADS scales at wave 2, a set of regression analyses was conducted, with wave 2 RCADS SAD, GAD, SoPh, PD, and OCD scores as dependent variables. These analyses were conducted to investigate how much of the variance in a specific RCADS scale score at wave 2 was not accounted for by its own counterpart at wave 1, but instead, by the other wave 1 anxiety scale scores. We will now describe the regression analyses that were conducted for wave 2 SAD. Those for GAD, SoPh, PD, and OCD were similar. In the first block of the analyses, wave 1 SAD scores were entered as predictor. Then, in the second block, scores on wave 1 GAD, SoPh, PD, and OCD scales were added, to see how much of the variance in wave 2 scores was specifically predicted by other RCADS scales at wave 1. This variance reflects specific heterotypic continuity. In the third block, sex was added.
To judge the magnitude of effects, Cohen’s rules for effects sizes can be used (Cohen, 1988). According to Cohen, R2 between 1.0% and 5.9% is small, between 5.9% to 13.8% medium, and above 13.8% large.
Results
Means and standard deviations at wave 1 were calculated for SAD (mean=.375, SD=.356), GAD (mean=.666, SD=.454), SoPh (mean=.779, SD=.427), PD (mean=.428, SD=.363), and OCD (mean=.597, SD=.445). Means and standard deviations were also calculated for wave 2 SAD (mean=.236, SD=.291), GAD (mean=.485, SD=.427), SoPh (mean=.684, SD=.465), PD (mean=.301, SD=.321), and OCD (mean=.339, SD=.348). Means reflect mean item scores for each RCADS scale.
Correlations among wave 1 RCADS scale scores for each sex separately are presented in Table 2. It is shown that all correlations were in a close range, almost similar across sexes, and generally above .50 which can be regarded as high (Cohen, 1988). For both sexes the highest correlations were found between PD and OCD (r=.61 in boys and girls), and the lowest between SAD and OCD (boys r=.47; girls r=.51).Table 2Correlations among wave 1 RCADS scale scoresWave 1 RCADS scaleWave 1 RCADS scaleGAD b/gSoPh b/gPD b/gOCD b/gSAD.52/.58.52/.52.51/.52.47/.51GAD—.59/.54.55/.54.58/.58SoPh—.56/.55.54/.53PD—.61/.61OCD—Note. Correlations are presented for boys (b), girls (g) separately.Table 3Correlations between wave 1 and wave 2 RCADS scale scoresWave 1 RCADS scaleWave 2 RCADS scaleSAD b/gGAD b/gSoPh b/gPD b/gOCD b/gSAD.30/.38.23/.32.35/.29.28/.27.21/.25GAD.27/.27.34/.38.29/.28.22/.25.23/.27SoPh.29/.29.35/.29.42/.41.29/.28.25/.25PD.22/.29.25/.31.24/.27.32/.42.25/.29OCD.23/.30.25/.32.28/.27.27/.32.31/.37Note. Correlations are presented for boys (b), girls (g) separately.
Correlations between wave 1 and wave 2 RCADS scale scores can be found in Table 3. For instance, in boys, the correlation between wave 1 and wave 2 SAD scores was .30, whereas the correlations between wave 1 GAD, SoPh, and PD scores and wave 2 SAD scores were .27, .29, and .22 respectively. Hence, heterotypic correlations were almost as high as the homotypic correlation. In girls, a similar result was found for wave 2 SAD. Heterotypic correlations ranged between .27 and .29, whereas the homotypic correlation was .38. Similar relatively small discrepancies between homotypic and heterotypic correlations were found for wave 2 GAD, SoPh, and PD scores.Table 4Specific homotypic continuity (prediction by target scale). Prediction of wave 2 RCADS scale scores by wave 1 scale scores and sexWave 2 RCADS scaleSADGADSoPhPDOCDWave 1 predictorsR2/F change/p1R2/F change/p1R2/F change/p1R2/F change/p1R2/F change/p1Non-target scales (block 1).119/69.68/.000.150/91.19/.000.132/78.35/.000.126/74.19/.000.106/61.22/.000Target scale (block 2).050/123.57/.000.023/58.06/.000.069/178.54/.000.037/90.39/.000.025/59.20/.000Sex (block 3).023/58.92/.000.036/93.32/.000.037/100.65/.000.032/81.21/.000.009/21.34/.000Target-scale*sex (block 4).001/2.06/ns.002/5.12/.024.000/.81/ns.009/23.81/.000.002/5.38/.020Models for girls/boys separately in case of interaction target-scale*sex Girls  Non-target scales (block 1)—.145/44.70/.000—.128/38.75/.000.109/32.82/.000  Target scale (block 2)—.024/31.06/.000—.060/77.54/.000.038/47.13/.000 Boys  Non-target scales (block 1)—.136/39.32/.000—.107/29.72/.000.089/24.41/.000  Target scale (block 2)—.018/20.85/.000—.020/22.82/.000.021/23.05/.000Note. Target-scale---Wave 1 RCADS scale identical to the wave 2 RCADS outcome scale in the regression model (prediction indicating specific homotypic continuity). Non-target scales---all other wave 1 RCADS scales, not identical to the wave 2 RCADS outcome scale. R2---explained variance.
The results of the regression analyses are presented in Tables 4 and 5. Analyses that were aimed at assessing specific homotypic continuity (Table 4) indicated that variances reflecting homotypic continuity were 2.3% for SAD, 3.6% for GAD, 3.7% for SoPh, 3.2% for PD, and .9% for OCD. Analyses aimed as specifically investigating heterotypic continuity revealed variances of 2.0% for SAD, 4.2% for GAD, 1.3% for SoPh, 2.3% for PD, and 2.7% for OCD (Table 5).
In analyses aimed at homotypic continuity, some anxiety*sex interactions were significant. A marked sex difference was found for PD. Table 4 shows that homotypic continuity was much stronger for girls (homotypic R2=6.0%) than for boys (homotypic R2=2.0%).
Discussion
The present study assessed homotypic and heterotypic continuity of symptoms of separation anxiety disorder, generalized anxiety disorder, social phobia, panic disorder, and obsessive compulsive disorder in individuals from a community sample, who were assessed for the first time when they were aged 10 to 12 years, and for the second time two years later. Variances reflecting homotypic continuity were roughly equal to those reflecting heterotypic continuity for SAD (2.3% versus 2.0%) and GAD (3.6% versus 4.2%). Variances reflecting homotypic continuity were larger than for heterotypic continuity for SoPh (3.7% versus 1.3%) and PD (3.2% versus 2.3%), and smaller for homotypic than for heterotypic continuity for OCD (.9% versus 2.7%) (Tables 4 and 5). Applying cross-sectional research designs, previous studies found high comorbidity rates among different types of anxiety problems (Essau et al., 2000; Masi et al., 1999; Newman et al., 1996; Verduin & Kendall, 2003). The present study extended the knowledge about the taxonomy of anxiety problems in young adolescents with longitudinal data. In accordance with previous cross-sectional work, SAD, GAD, SoPh, PD, and OCD symptoms appeared to be intertwined in a longitudinal fashion as well. However, considerable homotypic continuity was found as well.
Separation anxiety
For SAD, homotypic and heterotypic continuity were roughly equal. Previous studies indicated considerable comorbidity between SAD and the other anxiety problems, especially with SoPh (Compton et al., 2000). In the present study comorbidity rates at wave 1 were high as well, not only with SoPh, but also with other types of anxiety. This suggests that SAD and the other anxiety problems may represent two sides of the same coin. However, homotypic continuity was as strong as heterotypic continuity, which supports the usefulness of SAD as a separate diagnostic construct. The distinction between SAD and other types of anxiety was further supported by another study, in which we conducted latent class analysis to assess the boundaries between SAD and SoPh in referred 8- to 11-year-olds (Ferdinand et al., 2006). Four different classes of individuals were detected; those with (1) low SAD and SoPh item scores on a self-report questionnaire, (2) high SAD and high SoPh item scores, (3) high SAD and low SoPh scores, and (4) low SAD and high SoPh scores. This also supported the idea that, despite high comorbidity rates, SAD may at least partially represent a separate phenomenon, that, for instance, may be subject to specific etiological influences that differ from influences that affect the course of other anxiety problems.Table 5Specific heterotypic continuity (prediction by non-target scales). Prediction of wave 2 RCADS scale scores by wave 1 scale scores and sexWave 2 RCADS scaleSADGADSoPhPDOCDWave 1 predictorsR2/F change/p1R2/F change/p1R2/F change/p1R2/F change/p1R2/F change/p1Target scales (block 1).391/373.39/.000.375/337.53/.000.436/483.57/.000.380/347.98/.000.337/263.45/.000Non-target scale (block 2).020/83.77/.000.042/86.59/.000.013/103.79/.000.023/80.00/.000.027/82.20/.000Sex (block 3).027/81.60/.000.041/90.95/.000.040/107.45/.000.028/82.80/.000.012/55.90/.000Note. Target-scale---Wave 1 RCADS scale identical to the wave 2 RCADS outcome scale in the regression model. Non-target scales---all other wave 1 RCADS scales, not identical to the wave 2 RCADS outcome scale (prediction indicating specific heterotypic continuity). R2---explained variance.
Generalized anxiety
For GAD, homotypic continuity was almost as strong as heterotypic continuity. This is—at least partly—consistent with a previous study (Pine et al., 2001) in adolescents from the general population indicating that separation anxiety disorder and social phobia in adolescents did not predict future generalized anxiety disorder. This suggested rather strong homotypic continuity of GAD. However, continuity of GAD was more heterotypic than in the Pine et al. study, because in our study, heterotypic continuity was also considerable. This contrast may be due to methodological issues such as differences in sample characteristics (Pine et al. investigated older adolescents), assessment procedures (Pine et al. applied standardized interviews instead of self-report questionnaires), or statistical approach (Pine et al. used categorical diagnostic samples whereas the present study used dimensional scale scores). Further, Pine et al. did not use a block design for their regression analyses, but included all predictors in a forward stepwise logistic regression analysis. So, in essence, they did not test if one predictor predicted future GAD, over and above the effect of other predictors.
Social phobia
Compared to heterotypic continuity, homotypic continuity of SoPh symptoms was relatively strong. Pine et al. (2001) found that SoPh, but also GAD, in adolescence predicted future SoPh, independently of other types of anxiety, whereas SAD did not. Remarkably, in their study, GAD was a better predictor of future SoPh than SoPh itself. The aforementioned methodological differences between the Pine et al. study versus the present study may explain differences between findings.
Panic
Homotypic and heterotypic continuity of PD did not differ much. Analyses for boys and girls separately (Table 4) indicated that homotypic continuity was higher in girls than in boys. Previous studies already indicated that panic disorder tends to have a chronic course, in children as well as in adults (Biederman et al., 1997; Bruce et al., 2005). The prevalence of full blown panic disorder, and even of panic attacks, in adolescents is very low (Essau et al., 1999). The present study nevertheless suggests that in girls, the disorder may already begin with a chronic homotypic course at a very young age which is in accordance with the higher prevalence in females versus males (Goodwin et al., 2005), and with studies that retrospectively investigated age at onset, and that often point to childhood or adolescence as a starting point (Sheehan et al., 1981).
Obsessive compulsive disorder
Comorbidity rates of OCD with other anxiety disorders are generally high (Heyman et al., 2001; Tukel et al., 2002), which was supported by the correlations among the wave 1 RCADS scale scores. The present study showed that heterotypic continuity of OCD symptoms was higher than homotypic continuity. To our knwoledge, previous studies that assessed homotypic continuity of OCD symptoms versus heterotypic continuity with other types of anxiety in young adolescents are not available, so we cannot compare our findings with previous work. Homotypic continuity was somewhat stronger in girls than in boys. This seems to suggest that, longitudinally, OCD symptoms in boys correlate differently with comorbid conditions than OCD symptoms in girls. Again, we were not able to find previous work on this topic. Future studies are needed to investigate if the differences between boys and girls we found can also be found in other samples, countries, and cultures.
Practical implications
In many studies, anxiety disorders are treated as one group of disorders (Barrett et al., 2001; Lipman et al., 2001; MacMillan et al., 2001; Roza et al., 2003; Shortt et al., 2001), and, even, some widely used assessment instruments do not contain scales that tap different anxiety dimensions (Achenbach, 1991a, b). Previous studies found considerable associations between different types of anxiety symptoms, which suggested the presence of one higher order factor (Nauta et al., 2004). Several studies with adults also found evidence for a higher order factor that explained the presence of different types of anxiety (Hettema et al., 2005; Krueger, 1999; Vollebergh et al., 2001). Given the magnitude of heterotypic continuity in the present study, a higher order factor is likely to be present. However, the present study also showed that considerable homotypic continuity is present as well, occurring separately from a general propensity for high anxiety levels. This indicates that each type of anxiety problem may, at least partly, represent a distinct taxonomic construct. Homotypic continuity was found specifically for SAD, GAD, and SoPh, and for PD in girls. This may indicate that SAD, GAD, SoPh, and PD represent diagnostic constructs that are at least partially distinct. Hence, in clinical practice, instruments are needed that measure different anxiety dimensions separately. Intruments that just assess on single anxiety dimension may not be sufficient. Further, the distinctions between different anxiety constructs indicate that, despite the evidence that similar treatment methods are generally efficacious for different types of anxiety problems, each type of anxiety might require a slightly different treatment approach, and development of specific treatment modules.
Limitations
The sample consisted of young adolescents only. For older adolescents, different homotypic and heterotypic continuities could apply. Furthermore, questionnaires were used instead of clinical interviews; information about the presence or absence of DSM-IV (American Psychiatric Association, 1994) clinical diagnoses was not obtained. Even though RCADS symptom dimensions have proved to reflect corresponding DSM-IV anxiety disorders (Nauta et al., 2004), still, it may be the case that different results would have been obtained if DSM-IV diagnoses, that take account of the level of functional impairment, would have been used instead of RCADS scale scores.
Since different informants may provide different information, this study would have been more valuable if information regarding symptoms of different types of anxiety would also have been gathered from parents or teachers. Unfortunately, such information was not available.
Conclusion
In the present study’s sample of young adolescents from the Dutch general population, evidence for homotypic continuity was found, especially for symptoms of separation, social, and generalized anxiety, and for symptoms of panic disorder in girls.