Potential for internal recovery

As mentioned above, internal recovery depends upon the reproduction capacity and it is, therefore, linked to the generation time of a species. Thus, information on the life-cycle of species is considered crucial for understanding the recovery potential after toxic effects due to pesticides application.

Earthworms have been proven to produce eggs during the whole year. The eggs are contained in cocoons. If the soil is too dry, the cocoons are deposited deeper into the soil. Biomass and size of Figure 1: Representation of the main taxonomic groups of soil organisms on a body-width basis (Reprinted with permission from John Wiley and Sons after Swift et al., 1979) from Decaens (2010) and Barrios (2007) (all photo credits: Flickr, http://www.flickr.com/)

earthworm populations might be influenced by many parameters, including cocoons production which can be affected by seasonal variation in soil moisture, temperature, food supplies and other environmental factor, although earthworms can potentially produce cocoons throughout the year (Edwards and Bohlen, 1996).

It is well reported in the literature that few cocoons are produced in the winter period while the highest number is produced in the period May–July. Generally, the number of cocoons decreases with decreasing temperature, but the relationship is different for different species since the influence of environmental factors on population dynamics differs among earthworms of different ecological categories. Epigeic⁶earthworms, living and feeding mainly on the litter layer, may be more affected by seasonal temperature variations than endogeic⁷ or anecic species⁸ (those that inhabit permanent or semipermanent burrow systems in the soil) (Monroy et al., 2007).

Venter and Reinecke (1988) attributed to the availability and the quality of food as well as the maintenance of optimal moisture conditions a great importance for the growth rate of the E. fetida at 25°C. As shown in AppendixB,E. fetida displays in comparison to other earthworm species a relatively short life cycle with a high reproductive rate. Appendix B lists the life-cycle parameter for 12 Lumbricidae species. Total time for development ranges from 38 to 74 weeks.

Most land snails are oviparous and lay their eggs in clutches at sheltered places (e.g. soil cracks or burrows, under stones, among herbage (Barker, 2001). The number of eggs laid per clutch is highly variable within but also between species. According to Barker (2001), small terrestrial gastropods show a particular low fecundity, tending to produce only few eggs throughout their life (e.g. six in Punctum pygmaeum (Draparnaud) (Punctidae) during an average life span of 170 days). Larger animals may deposit several egg clutches per season (Kerney et al., 1983) and there often is considerable variation in the number of eggs per clutch and size of eggs within species, depending on the size and age of the parent animal, but also on environmental factors such as competition, and seasonality in climate (Barker, 2004). Mortality during the early life stage of terrestrial gastropods is rather high and it is not unlikely that only 5% or fewer animals of one egg clutch reach sexual maturity. Many terrestrial gastropods reach sexual maturity after 1 year, while the largest terrestrial gastropod species (but also some small species belonging e.g. to the genera Columella and Vertigo) may take 2–4 years to reach sexual maturity (Kerney et al., 1983).

Overall, it is concluded that especially smaller terrestrial gastropod species that make up the greater part of terrestrial gastropod diversity (see e.g. Sturm et al., 2006) are likely to have a poor recovery potential due to their low number of produced offspring and also their generation time may be rather long.

Most temperate species of isopods are seasonal breeders. However, there is a large variation in the period and duration of the breeding season. While some species breed in spring, others breed during the fall. Most species from temperate and Mediterranean habitats have breeding seasons lasting 4–8 weeks (Warburg et al., 1991), while others from tropical or temperate regions, the breeding season may last 3–6 months (Warburg, 1993). This is seen in tropical species Orodillo maculatus and subtropical species Bethalus pretoriensis that present a breeding season longer than for temperate species. The species Porcellionides pruinosus, however, represents an exception since it can breed continuously in tropical and temperate habitats.

Many woodlice species are iteroparous between years, i.e. they can produce more than one brood per year. Females of Porcellio scaber, for example, can produce up to three broods per year, whereas the species Porcellio laevis can produce up to six broods. This can vary also with the age of the individuals, and climate. In a warmer climate (California), first year females of Armadillium vulgare produce one brood within a year, while second year females can produce two broods. However, in East Anglia, the same species was semelparous. Fecundity in woodlice is associated with body size (Alikhan, 1995). Larger A. vulgare females can produce two broods per seasons, compared to one brood of smaller females.

The number of broods during a female life time can vary across species, going from one brood in certain populations of A. vulgare and other Armadillidiidae to more than six in populations of the species P. pruinosus and P. laevis.

6 Epigeic earthworms live within the litter layers.

7 Endogeic earthworms are unpigmented geophagous worms that live and feed within the soil’ (Lavelle and Spain, 2005).

8 Anecic earthworms feed on surface litter that they mix with soil but pass most of their time in subvertical subterranean galleries created within the soil’ (Lavelle and Spain, 2005).

Climatic parameters, such as temperature, can influence reproduction. Increased temperature shortened the development time for mancas⁹of Oniscus asellus and accelerated the reproduction in A.

vulgare (Warburg, 1993).

Mesofauna

Enchytraeidae species can reproduce either by sexual reproduction or asexually. For species able to reproduce sexually, adults lay cocoons that are a sort of mucilaginous bag, containing from 1 to 48 eggs. Hatching rate is usually high and can range from 19% to 97%. Enchytraeidae can produce 4–10 immatures per adult per year with a developmental period of 4–12 months in British meadow. A total life cycle in the range of 60–120 days from cocoon hatching to maturity has been reported under optimal conditions (Lavelle and Spain, 2005).

Westheide and Graefe (1992) reported life-cycle data for two species of Enchytraeids: Enchytraeus crypticus and Enchytraeus doerjesi. Burgers and Raw (2012) reported data from two sources on Enchytraeus albidus (see Table 1).

Asexual reproduction of Enchytraeidae occurs through fragmentation of individuals to form a few new ones, see Table 2.

According to species and size, Collembola species can have a number of stages going from 4 to 50.

Development through the reproductive instars can take 40 to 400 days and moulting occurs continuously over the entire life (Lavelle and Spain, 2005). The fecundity of collembolan females depends on the number of eggs laid in each clutch and the total number of clutches produced. A female of the species Sinella curviseta and Willowsia jacobsoni can produce an average of eight clutches with 50 eggs each during the entire life-cycle, under laboratory condition and with continuous access to a male. Overall, collembolan species have been reported to lay 100–600 eggs during the entire life time, which is around 1 year (Lavelle and Spain, 2005).

Embryo development takes about 10 days for the species Tomocerus ishibashi. For the species Entomobrya nivalis, egg development has been reported as taking 25 days at 9°C, 15 days at 13°C and only 7 days at 20°C.

The maximum life span for a springtail under controlled conditions is 5–7 months for the species Pseudosinella impediens. However, under realistic conditions, some species can live longer, especially in stable cave environments. The complete life cycle of Cryptopygus antarcticus may take from 2 to 7 years, since in very cold climates growth and reproduction are much slower.

Some species are univoltine while other can be multivoltine. For example, the species Tomocerus cuspidatus is univoltine with a short breeding period in spring, while the species Entomobrya aino is multivoltine.

Table 2: Life-cycle data on two species of Enchytraeidae (asexual reproduction)

Species No of

fragments

Development time to a

complete worm (days) Reference

Enchytraeus fragmentosus 3–14 10 Lavelle and Spain, 2005

Cagnettia sphagnetorum* 2–3 8–26 Lavelle and Spain, 2005

*: This species starts to fragment when individuals have more than 42 segments.

Table 1: Life-cycle data on three species of Enchytraeidae (sexual reproduction)

Species

Enchytraeus crypticus 9.06^(a) 8.3 81.6^(a) 0.62 7.6 4.6

Enchytraeus doerjesi 6.8 8.5 93^(a) 0.9 5.1 4.3

Enchytraeus albidus – 44.5/21 68.3/261 0.22/0.40 4–5/1–35

(a): Average of different values obtained for populations originating from different localities.

9 Young isopod crustaceans hatch directly into a manca stage, which is similar in appearance to the adult, but they lack the seventh pair of pereiopods. They undergo progressive moults of manca stages, two in general, until the complete development of the seventh pair of pereiopods and the beginning of the development of secondary sexual characteristics (Brum and Araujo, 2007).

Fountain and Hopkin (2005) reported for Folsomia candida an average life span for females of 240 days and 111 days at 15°C and 24 °C, respectively. The number of eggs laid by a female can decrease from 1,100 to 100 going from 15 to 27°C. An adult female may go through 45 moults in her lifetime with short reproductive instars (1.5 days) alternating to longer non-reproductive periods (duration 8.5 days).

At 20°C, the average duration of the five juvenile instars is 3 days for F. candida and maximum 4 days for F. fimetaria. Sexual maturity is attained in the 6th instar occurring around age 15–16 days for F. candida and a few days later for F. fimetaria. Egg development for F. fimetaria took 9.5 days, hence similar to 9–11 days observed for F. candida. Reproduction may be parthenogenic or bisexual.

Generally, it is reported that collembolans able to reproduce sexually, need fertilisation for every reproductive instar. With that regard, Krogh (2008) reported the result of a study aiming at following the oviposition pattern of reproduction. In that study, 24 couples of 25–28 days old, 8th instar, F. fimetaria males and females, and 24 single females were isolated and followed for 3 weeks at 20°C.

Single females did not produce any eggs and the couples produced 10 and 30 eggs in instars eight and ten, respectively, with a maximum clutch size of 60 eggs. In the same situation, for F. candida, 48 and 71 eggs were produced with a maximum clutch of eggs of 114.

Responses of soil organism communities after lindane application were investigated in a Terrestrial Model Ecosystem (TME) study. Collembolans were adversely affected by moderate dosages of lindane in terms of total and species-specific abundance as well as the community endpoints (principal response curves, diversity measures). Recovery was observed within 1 year (Scholz-Starke, 2013).

For acari, the post-embryonic development can take several months. Acari belonging to the Mesostigmata group have only two immature stages before moulting to the adult form. The other three non-parasitic orders (Prostigmata, Astigmata and Cryptostigmata) have six different developmental stages. Inactive forms are very common in acarine population. For example, Cryptostigmata can spend 30% or their annual cycle in moulting or resting stages. Most Cryptostigmata have one generation per year, although larger species or those living in boreal and arctic environments can take 2–3 years to complete their life-cycle. Reproduction is generally bisexual, although some species can reproduce via parthenogenesis. Cryptostigmata females may produce one to six eggs on average which hatch one to 6 weeks later. For Prostigmata, the number of eggs can vary from 10 to 100 depending on the species.

Oribatid mites are usually reported as having long life cycles, extended development, adult longevity, and iteroparity. The time for completion of an oribatid mite’s life cycle is dependent on temperature, moisture and the availability of food, and can vary from 5 months to 2 years. In general, small oribatid mites in a warm climate will take less time to complete a life cycle. In field studies conducted in temperate climates, most oribatid mites have shown a generation time of 1 or 2 years (Jordan, 2001).

Acari of the species Hypoaspis aculeifer (Acari: Mesostigmata), the standard test species, become sexually mature after 16 days (females) and 18 days (males). A life span between 48 and 100 days at 25°C is reported (OECD, 226).

Microfauna

In several studies, pesticides contributed to the declining diversity and complexity of nematode communities as reported by different specific indices (structural index (SI) and enrichment index (EI)).

Moreover, specific nematode genera were indicated as sentinels for recovery and describing the impact of soil management or land-use change. Mesorhabditis spp. was a consistent indicator of nutrient enrichment (Zhao and Neher, 2013; Malherbe and Marais, 2015). The resilience of Cephalobus spp. to tillage and other agricultural practices was enhanced (Fiscus and Neher, 2002) and Helicotylenchus spp. were identified as a candidate soil-health indicator in the tomato agroecosystem studied (Malherbe and Marais, 2015). In general, species of larger body size, such as the longer living, K-selected predaceous nematodes that are somewhat slower moving, would require more time to recover from stress, e.g. PPPs exposure and a larger water film around soil particles (which could also depend on the PPPs applied) to maintain their activity, compared to nematodes in other trophic groups, such as smaller sized, faster moving bacterial feeders with r-selected life strategies (Yeates et al., 2002). Plant parasitic nematodes are rather reactive but can be either target or non-target, depending on the PPP applied. Indirect measures of the resilience and natural attenuation of nematode communities are different traits of their ecological succession, including the fungivore to bacterivore ratio, maturity, and other ecological indices (Ferris et al., 2001).

Timper et al. (2012) found out that nematicides reduced numbers of all trophic groups compared to the control; for bacterial and plant feeders, there was also a consistent, lingering effect of the nematicides the following year at prefumigation. Interestingly, omnivores and predators were not severely impacted by the nematicide treatment; populations of both groups repeatedly recovered by

the following spring from the yearly application of nematicides, with the exception of predators in some cases. The authors highlighted also that the nematicides may have altered the soil community to allow a fungal, bacterial, or invertebrate antagonist of nematodes to increase in abundance, leading to an increase in suppressive service. In addition, although Caenorhabditis elegans is a bacterivorous nematode that exhibits exceptional resilience to adverse environmental conditions and different stress, protocols are now available to quantify its resistance to a variety of biotic and abiotic stressors (Keith et al., 2014). This could be a potential tool to estimate the potential recovery and consequent natural attenuation done by bacterivorous nematodes.

Soil microorganisms

Due to their specific traits and short generation time, it has been possible to study internal recovery of microbial populations or communities after exposure to PPPs relatively often. It has been demonstrated and reported (Puglisi, 2012) that microorganisms are often able to recover quite fast from toxic effects after exposure to pesticides. Those effects can be both at the structural and functional levels of the microbial community, as demonstrated by the heterogeneity in the measured and reported endpoints: abundance (number of cells or spores) and biomass (often recalculated from respiration measurements), physiological parameters (e.g. CO2 evolution, net nitrification or mineralisation), measurements of enzyme activities, differences in the structure (PCR-DGGE, PLFA, etc.).

Recovery after pesticide application was reported as occurring from 28 days after application (effects on dehydrogenase) to 114 days (effects on colony forming unit for fungi) (see Appendix C).

Some studies have also reported an adaptive response of soil bacteria as shown by the faster recovery of enzymatic activity after repeated applications of a pesticide (Yu et al., 2006; Imfeld and Vuilleumier, 2012). This could be explained by an enhanced mineralisation capacity acquired by the soil microbial community, and by other adaptive changes allowing the microbes to cope with the pesticide.

For mycorrhizae, little information is reported about their potential for internal recovery. Abd-Alla et al. (2000) investigated the effects of the pesticides pyrazophos (fungicide), bromoxynil (herbicide), paraquat (herbicide) and profenofos (insecticide) on arbuscular mycorrhizal (AM) spore number and root colonisation of the legumes cowpea (Vigna sinensis L.), common bean (Phaseolus vulgaris L.) and lupin (Lupinus albus L.). In the case of cowpea plants and common bean, the proportion of root length colonised by AM fungi was significantly decreased with all pesticides used 20 days after planting, but recovery from effects after the application of pyrazophos and bromoxynil was demonstrated after 60 and 40 days, respectively. However, root colonisation of lupin with AM fungi was significantly reduced with all pesticides. The number of AM spores sieved from the rhizosphere of cowpea was significantly decreased with all pesticides after 20 days, but the effect of paraquat had disappeared after 40 days.

Except for pyrazophos after 20 days, all the other pesticides significantly reduced the number of AM spores collected from the rhizosphere of common bean after all experimental periods. AM spore formation in the rhizosphere of lupin was inhibited with all pesticides and after all experimental periods.

3.2.2. Potential for dispersal