Introduction

Massive seasonal invasion of huge aggregations of litter dwelling darkling beetles Luprops tristis Fabricius 1801 (Coleoptera: Tenebrionidae), following summer showers and their prolonged stay in a state of dormancy (oligopause) is a seasonal nuisance for farming communities in the rubber plantation tracts of Kerala along the western slopes of the Western Ghats (Sabu et al. 2007, 2008). Clusters of several thousands of invading beetles crawl inside living rooms and often fall off from ceilings. Subsequently they congregate in dark, undisturbed areas such as attics and wall voids and remain dormant for nine months. They do not sting or bite, however, when disturbed (such as picking them off the walls or when they are squashed or pressed against while sleeping) they release an irritating odoriferous phenolic secretion that causes burns on the skin. With their detritivorous habits, harmless nature, nocturnal surface activity and diurnal passivity in lower litter layers, they would have remained inconspicuous facilitators in litter decomposition and nutrient cycling in monoculture “rubber forests” in the region. However, their massive seasonal invasion into traditional tile roofed residential buildings and thatched sheds make them the most dreaded beetles in rubber-growing regions.

L. tristis beetles breed in the litter stands of rubber plantations and all feeding stages have a strong preference towards tender leaves. Larval, pupal and teneral adult stages were observed in the field only after annual leaf fall and biology studies indicated that their life cycle is linked to the phenology of leaf shedding of rubber plants (Sabu et al. 2008; Joby 2006). Understanding the relationship between the phenology of leaf shedding of rubber plants and L. tristis is central to understanding its life history and population dynamics. Population management depends on accurate forecasting of seasonal activity and insect phenology, which deals with the timing of recurring biological events in relation to key environmental factors, is fundamental to understanding population growth and insect migration behaviour. Knowledge of the phenology of host and pest beetles may allow prediction of the timing of appearance of particular developmental stages in the field and requirements for life stage development, that may have potential for management (Nahrung and Allen 2004; Tauber and Tauber 1976). Here we present the results of two years of field monitoring of life stages, abundance patterns and timing of invasion and how the leaf phenology of rubber and the population dynamics of different stages of L. tristis are related.

Methodology

Sampling

The chronology of leaf phenology including leaf shedding, refoliation involving sprouting and new leaf flush, maturation, premature leaf fall, flowering and flower fall of 625 plants in a 100 m × 100 m plot were monitored weekly from December to May of 2004–05 and 2005–06. The percentage of trees in each phenology class was recorded each week.

Activities of aggregated, dormant beetles in thatched buildings in the vicinity of the study plot were observed on a weekly basis following post rainy invasion of beetles in April 2004 and April 2005. Earlier studies (Sabu et al. 2008) showed that L. tristis returns to rubber litter following annual leaf fall in rubber plantations in the second week of December. Abundance of L. tristis beetles in plantations following their return was checked for six months from the first week of December to the last week of May in 2004–05 and 2005–06.

Figure 1.

Rainfall data recorded during 2004–2006 study period at Thamarassery (All values in mm).

Leaf litter present inside a 1 m² area was collected by placing a 1 m² wooden quadrat frame onto the litter and then scraping up all litter and loose humus from within the frame area into a large polyethylene bag. Litter collected for analysis refers to the upper organic litter plus the loose humus layer. Samples for the extraction were kept undisturbed in the polythene bags, individual beetle stages were extracted employing Winkler sifting methods (Besuchet et al. 1987). Each sample was sifted through a wire sieve with square holes of 1 cm × 1 cm into a 2 m² white plastic sheet. Adults and larvae were hand picked in the order of fast moving larvae and adults followed by immobile pupae and dead adults and transferred to 70% alcohol in labelled containers. Abundance of each stage (identified as larvae, pupae, teneral adults and post dormancy adults) per 1m² of litter sample was recorded. Individual larval instars were not considered due to the small size and short duration of 1^st and 2^nd larval instars and the absence of external features to distinguish the stages. Larvae were categorized into stage 1 (< 6mm) and stage II (≥ 6mm) based on size. All adults collected up to the field presence of pupae were categorized as parental adults and those present afterwards were categorized into parental and teneral adults based on rigidity of elytra, which was determined by compressing the elytra laterally between a pair of forceps (Nahrung and Allen 2004). Sexing of adults was done following the sternal notch methodology (Vinod et al. 2008). Field appearance of parental adults was recorded in relation to annual leaf shedding and of larvae, pupae and teneral adults in relation to new leaf flush. Thirty samples of litter were collected per week at random from the plantation, maintaining sampling intervals of 10 m between samples. Time of sampling was between 18:30 h and 20:00 h when the beetles were active in field. Diurnal sampling was not done, as beetles were less obvious in the field as they were hiding behind leaf litter and stones.

Results

Leaf fall

Most trees (82% in 2004–2005 and 78% in 2005–2006) started litter fall in 2^nd week of December. Three percent of the trees in 2004–05 and 1% in 2005–06 started leaf shedding one week earlier (1^st week of December), 15% in 2004–2005 and 21% in 2005–06 started one week later (3^rd week of December). Sixteen per cent of the trees completed leaf shedding in the 4 week of December in 2004–05 and 14% in 2005–06. More than 95% of the trees completed leaf shedding in the 1^st week of January itself (99% in 2005 and 96% in 2006). The remaining trees (1% in 2005 and 4% in 2006) completed leaf shedding by the 2^nd week of January (Figures 2, 3).

Figure 2.

Phenology of leaf fall, leaf flush and flowering in a rubber plantation at Thamarassery during 2004–2006 study period. Numbers on the X axis are weeks. Values on the Y axis in percentage.

Dark green leaves

Light green leaves of 4% of the trees turned dark green in the 2^nd week of January in 2005 and 2% in 2007. Light green leaves of more than 75 % of the trees turned dark green, two weeks following sprouting (4 week of January), (82% in 2005 and 78 % in 2006), and entire trees turned dark green, three weeks following sprouting (1^st week of February). Powdery mildew mediated premature leaf fall was recorded throughout the flowering stage and the highest level of premature fall was observed 8 weeks following new leaf formation (2^nd week of March) in both study periods.

Fleure 3.

Population dynamics (mean ±SD) of each life stage (larvae (small), larvae (large), pupae, adult (post) and adult (pre)) collected per m² of litter in relation to the phenology of leaf fall and leaf flush in a rubber plantation at Thamarassery during 2004–2006 study period.

Population biology of L. tristis

From April to December, beetles were dormant and remained aggregated without any physical activities within shelters. No beetles were recorded in the litter of the plantation during the period. Arousal from dormancy and attraction towards light and nocturnal activity (refractory phase) was noticed in the 4 week of December and lasted for three weeks (15–17 days).

Overwintered parental beetles were recorded in the leaf litter two weeks following the beginning of annual leaf fall (4^th week of December to the 1^st week of March) (Figure 3). Abundance of beetles gradually increased and peaked 2 weeks following complete leaf fall and one week following new leaf formation (3^rd week of January) and declined 3 weeks following leaf fall (4^th week of January). Significant variation in weekly abundance was observed between as well as within sampling years (between years df = 1, F = 88.53, P <0.05; among weeks df = 9, F = 426.6, P <0.05). Parental adults were not recorded beyond 10 weeks following their field return (March 2^nd week). Dead parental adults were recorded in sifted samples 4 weeks after field return (4^th week of January) and their numbers peaked 5–6 weeks following return to plantations (2^nd week of February in 2005 and 1^st week of February in 2006). During both study periods (2005 and 2006), parental adults returned to the field two weeks following the beginning of annual leaf fall, peaked and declined during the same period (Figure 3). The sex ratio of post dormancy adults was 1:1.3 (male:female).

Figure 4.

Different stages of leaf phenology in RRII 105 plantation, a) Annual leaf fall, b) New leaf sprouting and tender brown leaf, c) Green leaf formation and powdery mildew affected light green leaf and d) Dark green leaf and flowering stage and powdery mildew affected dark green leaf. Inset images shows 1. Tender brown leaves, 2. Powdery mildew affected light green leaves and 3. Powdery mildew affected dark green leaves.

Teneral adults

Teneral adults appeared six weeks following new leaf formation (4^th week of February) in both the years when the plantations were in light green leaves. Their abundance peaked 11 weeks following new leaf formation (1^st week of April) in 2005 and 10 weeks following new leaf formation (4 week of March) in 2006. Two way ANOVA results showed significant variation in weekly abundance of teneral adults (between years df = 1, F = 520.24, P <0.05; among weeks df = 7, F = 1170.28, P <0.05). Their abundance declined drastically during 1^st week of April in 2005 and 4^th week of March in 2006 after the onset of summer showers. No beetles were recorded two weeks following summer shower (4^th week of April in 2005 and 3^rd week of April in 2006). Sex ratio of teneral adults was 1:1.08 (male and female).

Figure 5.

Leaf litter of rubber plantation during the leaf sprouting and flowering phase, a) Lower leaf litter layers with late stages of Vth instar larvae, larval exuviate and pupae, b) & c) Luprops trisits fed light green leaves and untouched dark green leaves in leaf litter and d) leaf litter with fallen flowers.

Discussion

This study reveals that by tracking the phenology of leaf fall in rubber plantations, timing of return of post dormancy adults of L. tristis and relating these with the onset of summer rainfall enables the prediction of the seasonal appearance of subsequent developmental stages of L. tristis in plantations, the timing of their invasion into buildings and the intensity of population build up in rubber plantations. The stages of rubber plant growth, with sprouting, new leaf production, flowering and leaf fall are spread over four months. Feeding stages of L. tristis peak in abundance when the resource (premature leaves) they exploit is most abundant. The data show the coincidence of the return of parental adults from buildings to the field with annual leaf shedding and the oviposition phase of parental adults with leaf sprouting. Tender leaf fall and prolonged premature leaf fall during the presence of larval and teneral adult stages in leaf litter must enhance the reproductive efficiency of parental adults, survival of early developmental stages and of new generation adults during dormancy. Hence, timing of both annual and premature leaf fall, with the appearance and duration of developmental life stages in leaf litter strongly influences the population dynamics of L. tristis.

The termination of dormancy and return to the field of post dormancy adults perfectly coincided with the end of annual leaf fall and fall of sprouting leaves in rubber plantations. It appears that rubber trees and dormant beetles may respond to the same environmental cue; rubber trees shed leaves well in advance of the onset of the dry season as a mechanism to prevent water loss (Santiago et al. 2004; Santiago and Mulkey 2005) and the return of dry conditions possibly leads to the arousal of L. tristis from dormancy (Sabu et al. 2008). This synchrony of termination of dormancy and subsequent field return of beetles with annual leaf fall and availability of prematurely fallen tender leaves is suggested as significantly contributing to the unprecedented abundance of L. tristis which is unheard of in natural or monoculture litter stands. It appears that L. tristis synchronises dormancy termination with annual leaf shedding and new leaf flush, which occur concurrently in plantations. Further, dormancy during the six month monsoon period, when litter habitat is less conducive for beetles, being wet and in the advanced phases of faster decomposition Joby 2006), allows synchronization of the L. tristis life cycle. It enables synchronized development of post dormancy adults irrespective of age class variations in the following dry season when the leaf litter habitat becomes suitable by the influx of fresh litter and the availability of tender leaves as a food resource. The simultaneous return of post dormancy adults to the litter habitat facilitates synchronized feeding and preparation for breeding activities through temporal and spatial coincidence of mates. Dormancy in L. tristis becomes a classical example of how seasonal patterns of development optimize reproductive efficiency by synchronising mating (Denlinger 1986) and food availability. Synchronized development of feeding stages with fresh fallen leaves enables efficient utilization of the tender leaf resources that are transient in nature, and the brief period of dry litter habitat provide conditions for larval, pupal and teneral adults before the onset of the long wet season.

Premature leaf fall occurs at two stages, the first at the time of leaf sprouting coinciding with the return of fooddeprived post dormancy adults and, later when larvae and teneral adults are abundant in leaf litter, ensuring that all feeding stages are in receipt of a continuous supply of preferred leaf resources. Furthermore, fallen flowers are another resource available to the beetles for a brief period of 5 weeks. Based on the strong preference of all feeding stages towards premature leaves (Sabu 2007; Sabu and Vinod in press), we suggest that control of powdery mildew-mediated premature leaf fall Jacob 2002) will limit the availability of tender leaves to larval stages and teneral adults. Implications of the limited availability of tender leaves to various developmental stages need to be experimentally ascertained to understand whether control of powdery mildew disease mediated premature leaf fall would enable regulation of the population build up of L. tristis beetles in rubber belts.

The presence of dead parental adults in litter samples, even when prematurely fallen leaves are readily available and a significant proportion of the larval population exists in the field, indicate that parental adults reached the end of their nine month long life span (Sabu et al. 2008). This observation substantiates the earlier findings that adults are univoltine and the longevity of L. tristis ends 5–7 weeks following their return to the field from dormancy (Sabu et al. 2008). The absence of dead larvae and teneral adults at any stage in leaf litter indicates that shortage of food resources is not affecting the population build up of the new generation and also their ability to survive in rubber leaf litter. Further, the decline of parental adults timed with the arrival of teneral adults and larvae avoids significant overlap of generations and competition for the preferred tender leaves.

The increase in the number of dead post dormancy adults in litter samples, four weeks following their return to the field, and one week prior to the emergence of larval instars, raises an important question about the relationship between the phenology of litter fall of different Hevea clones and habitat and feeding requirements of post dormancy adults. Among rubber clones cultivated in the region, the annual leaf shedding of RRII 105 alone coincides perfectly with the field return of L. tristis; for other clones leaf shedding starts two weeks later Joby 2006). Consequently, we speculate that in the absence of RRII 105 clones, post dormancy beetles would face a two-week delay in suitable litter habitat with which to start breeding activities. In the absence of RRII 105 plantations, delayed leaf fall by 2–3 weeks in other clones may lead to non-availability of suitable litter habitat and preferred tender leaves to post dormancy adults and consequently high early mortality of post dormancy adults and lesser reproductive efficiency of the surviving beetles. Currently, mating pairs are observed in the first week after the return of post dormancy adults, and eggs and first instar larvae appear in the second week after return, leading to the formation of a subset of teneral adults with a very long period of feeding time prior to their entry into dormancy. Dead parental adults were observed for a six week period (4^th week of January to 1^st week of March) even in the presence of readily available tender leaves at the time of their return to the leaf litter. Consequently, a 2–3 week (4 week of May) delay in getting a litter habitat and tender leaves is certain to affect the feeding and reproductive efficiency of post-dormancy beetles and the active feeding time available to teneral adults. It raises the question of employing rubber clones with delayed leaf falling pattern or utilizing the intraclonal variation in leaf shedding of RRII 105 clones as a cost effective control measure to reduce population build up of L. tristis. This study predicts that introduction of rubber clones whose leaf shedding does not coincide with post dormancy return of L. tristis and sheds litter later than RRII 105 clones will lead to low population build up of L. tristis, and the introduction of clones that shed leaves earlier to the post dormancy return of L. tristis will lead to rise in population build up of L. tristis. Two new clones, RRII 430 and RRII 414, introduced as replacements for the widely cultivated RRII 105, shed leaves 15 days later than RRII 105. How they affect the population build up and life cycle of L. tristis needs to be analyzed. Since RRII 105 is the most widely cultivated clone (Saraswathyamma et al. 2000) and young plantations of various ages are present in the region, RRII 105 plantations will provide a suitable habitat for L. tristis for another 10–15 years and switching over to new clones and the compete shutting out of the availability of timely litter habitat and tender leaves will be a gradual process. That leaves the control of premature leaf fall in the existing rubber plantations and limiting the availability of preferred food resources as a more practical option for the control of L. tristis, which needs to be experimentally tested.

The emergence pattern of teneral adults shows that there are six age-classes of teneral adults with those emerging in the 1^st week getting 6 weeks of feeding time, 2^nd week arrivals getting 5 weeks etc., whereas those in the last week before the onset of summer rains get hardly one week. The highest abundance of tenerals was recorded in the 1^st week of April in 2005 (five weeks after appearance in the field) and the 4^th week of March in 2006 (four weeks after appearance in the field). The highest formation of tenerals occurred two weeks following their appearance in both years (2^nd week of March) with a rise of 30.8% and 34.1 % in 2005 and 2006 respectively. Since the age class of tenerals varies based on their emergence date, those with a longer age class have more feeding time and hence more reserve food to tide over dormancy than the late developed short age class adults (Sabu et al. 2008). This supports the earlier findings that the duration of teneral adults before dormancy, the active feeding time available to them and the timing of onset of summer showers are the important factors deciding the population build up of L. tristis. Since field return of post dormancy adults, summer rainfall and home invasion of teneral adults occurred in the same period in 2003–04 Joby 2006), 2004–05, and 2005–06 (present study) periods, in the absence of empirical data we speculate that variation in the availability of prematurely fallen tender leaves might have lead to the differences in field abundance of beetles between years and not variation in the incidence of rainfall.

Analysis of the amount of fat body required to tide over the nine month period of dormancy and feeding duration required for sufficient build up of fat body needs to be measured to predict the effect of variable duration of feeding time in the life span of L. tristis. Our observations in the rubber belts of northern Kerala where intensity of aggregation is more severe than in south Kerala where arrival of summer rains (KDAF 2005; Vijayakumar et al. 2000) and subsequent beetle invasion is delayed six weeks, revealed that all field stages of L. tristis get six weeks more feeding time. Hence, the following sequence of events could possibly lead to comparatively very heavy increase of L. tristis in North Kerala: late onset of summer rains, entry of all larval and pupal stages into the adult stage from the absence of rainfall-mediated mortality, and the longer feeding time available for teneral adults of different age classes leading to greater consumption of reserve food materials by all age classes and increased survival during dormancy.

The total absence of larvae/pupae and the very low presence of adults in the field after the arrival of summer showers during both study periods indicate that rainfall is the most important factor driving them to dormancy and making it a very crucial event determining the life cycle of L. tristis in the region. The sudden disappearance and invasion into buildings following summer showers is not surprising as tenebrionids generally prefer dry habitats (Endrödy-Younga and Tschinkel 1993; Watt 1992) and present records shows that L. tristis is not an exception. However, it is not understood why they do not return to the field after the occasional showers in the first week of April/last week of March, which last for 5–10 days. Following summer showers, the leaf litter is dry for approximatly 45 days before the South West monsoon rains occur in June and the invading beetles could have returned to field instead of remaining in dormancy. We suggest that wetness “turns on” the irreversible physiological mechanisms to enter into dormancy (Mansingh 1971; Tauber and Tauber 1976; Denlinger 1986, 2002; Danks 1987; Leather et al. 1995) or probably, the perfect synchronism of L. tristis with rubber tree phenology/weather arose by means of natural selection.