Where Have All the Spiders Gone? Observations of a Dramatic Population Density Decline in the Once Very Abundant Garden Spider, Araneus diadematus (Araneae: Araneidae), in the Swiss Midland.

Aerial web-spinning spiders (including large orb-weavers), as a group, depend almost entirely on flying insects as a food source. The recent widespread loss of flying insects across large parts of western Europe, in terms of both diversity and biomass, can therefore be anticipated to have a drastic negative impact on the survival and abundance of this type of spider. To test the putative importance of such a hitherto neglected trophic cascade, a survey of population densities of the European garden spider Araneus diadematus-a large orb-weaving species-was conducted in the late summer of 2019 at twenty sites in the Swiss midland. The data from this survey were compared with published population densities for this species from the previous century. The study verified the above-mentioned hypothesis that this spider's present-day overall mean population density has declined alarmingly to densities much lower than can be expected from normal population fluctuations (0.7% of the historical values). Review of other available records suggested that this pattern is widespread and not restricted to this region. In conclusion, the decline of this once so abundant spider in the Swiss midland is evidently revealing a bottom-up trophic cascade in response to the widespread loss of flying insect prey in recent decades.


Introduction
When the Entomological Group Krefeld along with colleagues published their famous long-term study (the "Krefeld study") in 2017, it became known that the flying insect biomass had declined by approx. 75% over the past three decades in over 60 nature protection areas of Germany [1]. Another long-term study (the "Munich study") basically confirmed the results of the Krefeld study, providing evidence that strong abundance declines of insect populations had occurred in farmland and forests across vast areas of Germany and Switzerland [2]. Similar abundance declines of insect populations were documented by means of other long-term studies for other European and North American regions [3][4][5][6][7][8][9]. Meanwhile, it is generally accepted as scientifically proven that in many parts of the globe insect population densities had drastically decreased in recent decades and that we now live in an era of global insect meltdown [9][10][11][12][13]. This has dramatic ecological implications due to the fact that insects comprise the base of many food chains and food webs [14,15] in a world without insects countless insectivorous species would ultimately become extinct due to starvation [16].
In this context, aerial web-spinning spiders are a group of uttermost interest. This group of spiders (including the orb-weaving spiders in the families Araneidae) trap flying insects with the aid of aerial webs [17][18][19]. In the temperate climate zone, aerial web-spinning spiders feed for the most part on small dipterans, aphids, and hymenopterans ( Figure 1) which are exactly the type of insects known to have most dramatically decreased in abundance and biomass in recent decades [1]. With other words, because of their reliance upon flying insects as their principal food source, aerial web-spinning spiders are a highly vulnerable predator group in regions characterized by high loss of flying insects such as Germany and Switzerland.
While a larger number of studies on population declines of various groups of insects had been conducted in recent years (see references in [12]), potential cascading effects have been documented so far for insectivorous birds [6]. No studies of this type have so far considered potential declines due to trophic cascades among arthropods, like aerial web-spinning spiders. In the following we use the European garden spider Araneus diadematus as a model system to address the question whether evidence for population declines in aerial web-spinning spiders in the Swiss midland can be found.
The female, 10-18 mm in length, reaches adulthood in late summer, at which time it spins (≈30 cm Ø) orbs [20][21][22]. The webs are built 0.5-2.5 m off the ground [21]. This animal with its conspicuous white, cross-shaped mark on the upper side of the abdomen is one of the best known spider species in western Europe.
By comparing historical abundance data (20 th century) with present-day data (year 2019) it shall be examined whether the abundance of Araneus diadematus has changed over the past few decades. This work is based on extensive experience gathered during graduate research in the Swiss midland in the 20 th century [20,21] and has since been supplemented by a present-day population density survey in the same geographical area. To make the comparison more robust, the data base was expanded by adding published population density values extracted from the scientific literature.

Assessment of population densities of Araneus diadematus in 2019
Population density assessments were conducted on 20 locations in the Swiss midland by walking transects and counting webs (see Table 1, Table S1 for details). The search focussed on webs of adult females in its typical habitats (gardens, parks, graveyards, hedgerows, forest edges, forest trails, fallow grassland patches). Transects of 200 to 1000 m 2 ground area were used (area size depending upon the specific situation; see Table S1 for details). All counts were conducted on rain-free afternoons in August and September 2019.

Literature search for historical data on Araneus diadematus population densities
Araneus diadematus population density values assessed in the 1970s have been taken from two graduate research theses which had been conducted in the Zurich area [20,21]. These data were supplemented by data taken from the literature. Overall, a total of 12 reports (including 18 population density values) could be gathered (see Table S1). In these studies, transects ranging from 100 to 5000 m 2 ground area were used (see Table S1).

Statistical methods
The Mann-Whitney U test was applied to examine whether overall mean spider density in 2019 (N = 20) differed statistically significantly from overall mean spider density in the 20 th century (N = 18).
Mean values are followed by Standard Errors (± SE).

Results
In Table 1   In 2019, the webs appeared to be rather fragile (Figure 2A-B) compared with the stronger webs from previous decades, as is the case when malnourished spiders make webs with thinner threads (Nyffeler, pers. observations). This is in good agreement with laboratory experiments, in which the amount of produced thread was reduced if Araneus diadematus spiders were kept fooddeprived [23].
Furthermore, the webs contained few prey compared to previous studies (Table S2). The overall impression gained during this survey was that there was a paucity of prey throughout the entire study area in recent decades which is confirmed by the observations of other researchers [2,24,25].

Discussion
This study revealed that the large orb-weaving spider Araneus diadematus occurred in extraordinarily low population densities in the Swiss midland in 2019 (Table 1). Araneus diadematus spiders take down their webs during the night and rebuild them early in the morning. However, as laboratory experiments and field observations had revealed, not the entire population is rebuilding its webs the following day [23,26]. Some spiders, which had consumed exceptionally large amounts of food at particularly favorable hunting sites, may cease feeding and rebuilding their webs for one or several days [23]. Thus, the percentage of spiders found with webs within a A. diadematus population is in general lower than 100% (usually ranging between about 66-88%) depending on the availability of food at a particular time and location [23,26]. The question arises whether the method of web counts applied in this study may have resulted in underestimating the true population densities by overlooking a certain percentage of satiated spiders which had not rebuilt their webs at the time when the counts were conducted. On this issue, it may be noted that densities assessed in the past century were for the most part also based on web counts [18,20,21,[26][27][28][29][30][31][32] so that the same methodological bias was involved in both time periods. Furthermore, since insatiated spiders tend to rebuild their webs more frequently than fully satiated spiders [23,33], and since present-day spiders living in the era of insect loss are more likely to be insatiated compared with half a century ago (Table S2), the frequency of web building nowadays can be expected to be rather higher compared with the situation in the last century. Thus, the possibility that the extraordinarily low present-day population densities were underestimations due to this particular type of methodological bias can be ruled out.
The here documented abundance decline of this once so abundant spider in the Swiss midland is evidently revealing a bottom-up trophic cascade in response to prey scarcity recently documented in the Swiss midland and across vast areas of western Europe [1,2,24,25]. The hypothesis that the availability of flying insect prey in the study area had drastically declined over the past decades is confirmed by the "windshield phenomenon" noticed throghout the Swiss midland (i.e., nowadays many times less flying insects are killed on the front windshields of cars compared to previous decades; [9,34]. This is in sharp contrast to the situation a few decades ago, when fairly frequently "wasteful killing" (and coupled with it "partial consumption") of insects in Araneus diadematus webs at favorable web sites could be witnessed (with capture rates of sometimes up to 1000 prey web -1 day -1 ; [35]). The reduced food intake of Araneus diadematus in recent years (Table S2) is assumed to have negatively impacted the fecundity and survival of this spider [36,37) which in turn led to the abundance decline documented in this study (Table 1). Sublethal effects of chemical pollution may have additionally negatively affected this spider's survival [38][39][40][41][42][43].
Aside from food scarcity due to insect population declines and chemical pollution, other negative We of course realise that the recorded declines were not based on systematic long-term monitoring and that the declines could be attribited to normal population cycling. However, while we are not able to provide a smoking gun herein, several elements support a systematic decline. First of all, the dramatic decline up to <1% of the reference baseline from 40 years ago, has never been observed at shorter temporal time frames, and reach far beyond the typical natural fluctuations in population sizes (e.g., Green 2003), even when they are known to be linked to resource pulses (e.g., Wolf 1996).
Second, records from other location show that this decline is occuring at such large spatial scales that can only be explained by large-scale, more global environmental drivers like land-use change, climate change or the global use of pollutants. Indeed, the extraordinarily low population densities in Araneus diadematus in the Swiss midland observed in the 2019 survey (Table 1)  Interestingly, while other orb-weaver speciesespecially the larger onesshowed dramatic declines in both abundance and species richness along an urbanisation gradient [53,54], A. diadematus was found to reach similar low densities across this land-use gradient. Or put conversely, local densities at spatial scales of approximately 100 km were alarmingly low in both the more natural and human impacted regions, demonstrating regional declines beyond the scale of local land-use. Thus, extraordinarily low present-day population densities of Araneus diadematus have been recorded in two different regions of western Europe, ≈500 km apart. These declines extend local environmental changes at small scales and suggest common negative impacts of intensive urbanization, climate change or any other large-scale stressor across the entire landscape over the past half-century [55,56].
The present study and that from northern Belgium suggest that the notion that Araneus diadematus is an abundant spider, as pointed out in much of the literature [57,58], has these days turned out to be a mythat least in highly urbanized western European landscapes such as the Swiss midland and northern Belgium. But so far the apparent abundance decline of this species in western Europe had been ignored by faunists in charge of compiling local Red Lists for spiders (e.g., [57,58]). Red Lists are based on the number of different locations within a landscape from which a species has been recordedand not on absolute population densities, and the fact that Araneus diadematus is still found in many places (although in strongly reduced densities) may explain why it is still labeled as an "abundant species" (e.g., [57,58]).
In contrast, present-day population densities of Araneus diadematus in some areas outside of continental western Europe appear to be still rather high. So for instance, exterminators of the pest control firm Senske Services removed more than 75 Araneus diadematus spiders from the exterior of a "2,500-square-foot home" in Seattle (USA) in August 2016, which translates to a population density of 0.32 spiders m -2 [59]. Evidently the spiders at this particular location were still capturing a sufficient amount of food in the form of flying insects enabling them to build up a population density roughly 290 times that of the present-day Swiss overall mean density. Future detailed assessments of the population densities of this spider species in the different parts of its geographic range are urgently needed and may provide important clues on the extent of the loss of flying insects in various regions of western Europe and of the globe. We would in this respect like to promote the use of new citizinscience tools such as SpiderSpotter [60] to achieve these highly needed insights, and especially to guide short-term action to mitigate these alarming declines in these sentinel arthropod top-predators.

Concluding Remarks
The drastic decline in the abundance of the orb-weaving spider Araneus diadematus over the past half-century documented in this study (Table 1) is apparently revealing a bottom-up trophic cascade in response to widespread insect losses that had occurred across large parts of Europe in recent decades [1,2,4,6,9,25,61,62]. There is evidence that other groups of aerial web-spinning spiders, which likewise depend on flying insects as food [17][18][19]21,[63][64][65], have also become much rarer over the past decades (Nyffeler, pers. observations). So for instance, the mesh-web weaver Dictyna uncinata (along with other dictynid species) whose small, tangled webs were found in large numbers on the leaves of garden plants a few decades ago [65], has apparently become very rare these days (Nyffeler, pers. observations). The ongoing abundance decline of the spiders parallels the dramatic abundance declines in other insectivorous animals such as insectivorous birds, bats, frogs, and lizards documented in recent decades [66][67][68].
To sum this up, the findings of this study support the notion by other researchers that we now live in the midst of an ecological crisis in which trophic webs are being eroded and degraded as a result of man-made adverse environmental impacts [13,61,67,69,70]. If this disastrous trend cannot be halted or even reversed in the very near future, "entire ecosystems will collapse due to starvation" [16].

Conflicts of Interest:
The authors declare no conflict of interest.