Indirect nontarget effects of host-specific biological control agents: Implications for biological control

Classical biological control of weeds currently operates under the assumption that biological control agents are safe (i.e., low risk) if they do not directly attack nontarget species. However, recent studies indicate that even highly host-specific biological control agents can impact nontarget species through indirect effects. This finding has profound implications for biological control. To better understand the causes of these interactions and their implications, we evaluate recent case studies of indirect nontarget effects of biological control agents in the context of theoretical work in community ecology. We find that although particular indirect nontarget effects are extremely difficult to predict, all indirect nontarget effects of host specific biological control agents derive from the nature and strength of the interaction between the biological control agent and the pest. Additionally, recent theoretical work suggests that the degree of impact of a biological control agent on nontarget species is proportional to the agent’s abundance, which will be highest for moderately successful control agents. Therefore, the key to safeguarding against indirect nontarget effects of host-specific biological control agents is to ensure the biological control agents are not only host specific, but also efficacious. Biological control agents that greatly reduce their target species while remaining host-specific will reduce their own populations through density-dependent feedbacks that minimize risks to nontarget species.     

Biological studies on Trichogrammatoidea bactrae Nagaraja (Hymenoptera: Trichogrammatidae), egg parasitoid of Tuta absoluta Meyrick (Lepidoptera: Gelechiidae)

The tomato moth, Tuta absoluta Meyrick, is one of the most important tomato pests in South America. In Argentina, management strategies include only chemical control. In this work, the parasitoid wasp Trichogrammatoidea bactrae Nagaraja was evaluated as a potential natural enemy against this pest. Biological and population parameters were estimated by developing a life table under laboratory conditions at 25 ± 1oC, 14:10 photoperiod and 60 ± 10% RH. Three cohorts of 26-30 T. bactrae females each were placed with one of the three following treatments: 1 - Sitotroga cerealella (Olivier) eggs on a piece of cardboard; 2 - S. cerealella eggs on a piece of tomato leaf, and 3- T. absoluta eggs on a piece on tomato leaf. The following parameters were estimated for each cohort: survival (egg to adult), longevity, fecundity and oviposition period of females, sex proportion of the F1, net rate of reproduction (Ro), mean generation time (T) and intrinsic rate of population increase (r m). Survival of the T. bactrae immatures was higher than 90% on both, S. cerealella and T. absoluta eggs. The female survival curves corresponded to type III and showed no significant differences among treatments. The three cohorts did not show significant differences between sex ratio, female longevity, oviposition period, fecundity and the population parameters studied. These results indicate that T. bactrae would be a potential biological control agent of T. absoluta.     

The role of parasites in regulating host abundance

It has been 11 years since Anderson and May demonstrated the theoretical ability of helminth parasites to regulate host population abundance. In this review we consider how their work has advanced our understanding of the role of parasites in host populations. In particular Marilyn Scott and Andy Dobson consider three questions. What is meant by regulation? Is there empirical evidence that parasites can regulate host population abundance? Is it possible to predict the sort of host parasite association where one is most likely to be able to detect parasites as a major regulatory force?     

Indirect nontarget effects of host-specific biological control agents: Implications for biological control

Classical biological control of weeds currently operates under the assumption that biological control agents are safe (i.e., low risk) if they do not directly attack nontarget species. However, recent studies indicate that even highly host-specific biological control agents can impact nontarget species through indirect effects. This finding has profound implications for biological control. To better understand the causes of these interactions and their implications, we evaluate recent case studies of indirect nontarget effects of biological control agents in the context of theoretical work in community ecology. We find that although particular indirect nontarget effects are extremely difficult to predict, all indirect nontarget effects of host specific biological control agents derive from the nature and strength of the interaction between the biological control agent and the pest. Additionally, recent theoretical work suggests that the degree of impact of a biological control agent on nontarget species is proportional to the agent’s abundance, which will be highest for moderately successful control agents. Therefore, the key to safeguarding against indirect nontarget effects of host-specific biological control agents is to ensure the biological control agents are not only host specific, but also efficacious. Biological control agents that greatly reduce their target species while remaining host-specific will reduce their own populations through density-dependent feedbacks that minimize risks to nontarget species.     

Effect of temperature on parasitism and host-feeding of Trichogramma turkestanica (Hymenoptera: Trichogrammatidae) on Ephestia kuehniella (Lepidoptera: Pyralidae)

The egg parasitoid Trichogramma turkestanica Meyer is being evaluated as a biological control agent against the Mediterranean flour moth, Ephestia kuehniella Zeller, in flour mills. The longevity, parasitism and host-feeding of the parasitoid at four constant temperatures (15-30 degrees C) has been determined in the laboratory. The highest fecundity occurred at intermediate temperatures. The number of host eggs killed by host-feeding per female was highest at the two lower temperatures. A very conservative estimate of host-feeding showed that it accounts for approximately half of the mortality of host eggs at 20 and 25 degrees C and thus could constitute a major mortality factor for the flour moth population.     

Ecological role of control agent,and not just host‐specificity,determine risks of biological control

Biological control agents used to manage alien vegetation are generally viewed as providing an ecosystem service, owing to reduced ecological and economic costs of invasion following their release. In particular, gall‐formers are popular as biological control agents because they are host‐specific and therefore considered low risk. However, galls can also be considered to be ecological engineers, because they provide nutritional resources for native invertebrates. We tested whether native invertebrates had formed associations with the gall‐forming fungus Uromycladium tepperianum, introduced into South Africa to control the Australian invasive alien tree Acacia saligna, by collecting U. tepperianum galls and monitoring emergence. We found that a number of invertebrates had formed associations with the biological control agent, among which was the important citrus pest, Thaumatotibia leucotreta (false codling moth). We used pheromone‐baited traps to ascertain if this supplementary source of T. leucotreta increased their abundance in orchards close to patches of gall host, but did not find this to be the case. We did find, however, that control measures used by farmers explained T. leucotreta abundances in traps, which may have obscured detection of any effects of a nearby host for the pest. Nevertheless, this study illustrates the first case of a host‐specific classical biological control agent providing resources for an economically significant crop pest. We conclude that although biological control agents are strictly vetted to ensure host‐specificity, introduced biological control agents that become abundant and can act as ecological engineers pose risks when native biota form associations with them, resulting in a number of possible cascading ecosystem effects. In addition, there could be economic consequences when these associated species include agricultural pests. We conclude that not just host specificity, but potential ecological effects of biological control agents, should be considered in their selection.     

Effect of short-term high temperature stress on the development and fecundity of Ophraella communa (Coleoptera: Chrysomelidae)

Since insects are ectothermic, they are highly vulnerable to the sudden increase of temperature. Indeed, it has been hypothesized that the survival, development, fecundity, and even population expansion of insects are all affected significantly by extremely high temperature. We studied the effect of short-term high temperature stress on the survival and development of different stages, adult longevity and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a biological control agent of the invasive plant, the common ragweed, Ambrosia artemisiifolia (Asterales: Asteraceae) in the laboratory. The results showed that egg, larval, pupal and adult survival rates were significantly affected after 2 hour-short-stress at high temperatures (35 to 47°C) when compared to the 28°C control. With the exceptions of the control and 35°C stress, survival rate of females was significantly higher than that of males after short-stress at any high temperature. Short-term high temperature stress also significantly impacted longevity and fecundity of adult beetles. Except for control, female longevity was significantly longer than male's after short-stress at any high temperature. The survival rates of different stages, and adult longevity and fecundity of the beetle decreased significantly with the increase of short-term stress temperature. Based on the results of the present study, we conclude that the development and population expansion of O. communa may be significantly affected when they are exposed to a high temperature stage in a summer day in the areas invaded by common ragweed, in southern China.     

Effect of mating and parasitism regimes on progeny production and sex-ratio of Campoletis chlorideae Uchida

The ichneumonid parasitoid, C. chlorideae is an important natural enemy of pod borer/bollworm, Helicoverpa armigera (Hubner) in different agro-ecosystems. The sex-ratio of parasitoids has an important bearing on the population build up of the natural enemies for biological control of insect pests. Therefore, the present studies were conducted to gain an understanding of the influence of mating behaviour and abundance of the insect host on fecundity and sex-ratio of the parasitoid, C. chlorideae. There was no significant influence of number of matings and abundance of the insect host on cocoon formation, adult emergence, and larval and pupal periods of C. chlorideae. However, fecundity and female longevity were significantly influenced by mating and abundance of the insect host. There was a significant and positive correlation (r = 0.84**) between longevity and fecundity of C. chlorideae females. The unmated C. chlorideae females produced only males. Nearly 20% of the females that had mated twice were able to parasitize the H. armigera larvae successfully. The sex-ratio of the progeny from females that had mated twice was male biased. Females mated with males from the unmated females produced significantly less numbers of females than those mated with males from the fertilized females, indicating genetic regulation of sex-ratio in C. chlorideae.     

Early impact of endoparasitoid Microctonus hyperodae (Hymenoptera: Braconidae) after its establishment in Listronotus bonariensis (Coleoptera: Curculionidae) populations of northern New Zealand pastures

The South American curculionid Listronotus bonariensis (Kuschel) is an important pest of pastures in New Zealand. Population census data were gathered for L. bonariensis in northern New Zealand pastures during 1980-1983 in the absence of parasitism and again in 1991-1996 after the introduction and establishment of the braconid parasitoid Microctonus hyperodae Loan as a biological control agent. M. hyperodae achieved high rates of parasitism, with 75-90% of overwintering L. bonariensis parasitized within 3 yr of the parasitoid establishing at a site. Multistratum analysis of variance (ANOVA), with allowance for variation in host plant resource (numbers of Neotyphodium-free grass tillers), indicated reduction in the abundance of L. bonariensis life stages in the early part of life cycle. Although providing evidence for suppression of L. bonariensis, these analyses indicated the regulatory role of M. hyperodae was weak because L. bonariensis populations continued to exhibit marked intergenerational variability in abundance. Analyses of life tables indicated larval + pupal survival contributed most to intergenerational changes in abundance, irrespective of presence or absence of M. hyperodae. However, the density dependence of the stage survivals was modified in the presence of the parasitoid, with loss of density-dependent mortality in overwintering adults and increased density dependence in population natality. Regression analyses indicated dual contribution of parasitism and host plant resource to regulation of population natality and population trend in L. bonariensis. We conclude that M. hyperodae is a useful adjunct to host plant resistance in reducing the economic status of L. bonariensis populations in northern New Zealand pastures.     

Host diet as a determinant of parasite growth, reproduction and survival

Changes have been observed in the biology of protozoan and helminth parasites of small mammals during a variety of experimental nutritional manipulations ranging from deficiency in a specific nutrient to the general withholding of food from the host. Commonly observed effects include retardations in parasite growth rate, gametogenesis, fecundity, and asexual multiplication. The duration of patency and of the association of a parasite with its host have also been observed to be curtailed. The nutritional responses of parasites during host hibernation require investigation and much research will be needed to explain how perturbations in host dietary composition and intake may lead to the observed effects. Care should be exercised over applying the results from experimental studies to naturally occurring infections, but the experiments are justified because they indicate potential effects, if not their biological significance, and because causation can be determined.     

Coexistence of multiple parasitoids on a single host due to differences in parasitoid phenology

There are many well-documented cases in which multiple parasitoids can coexist on a single host species. We examine a theoretical framework to assess whether parasitoid coexistence can be explained through differences in timing of parasitoid oviposition and parasitoid emergence. This study explicitly includes the phenology of host and parasitoid development and explores how this mechanism affects the population dynamics. Coexistence of the host with two parasitoids requires a balance between parasitoid fecundity and survival and occurs most readily if one parasitoid attacks earlier but emerges later than the other parasitoid. The host density can either be decreased or increased when a second coexisting parasitoid is introduced into the system. However, there always exists a single parasitoid type that is most effective at depressing the host density, although this type may not be successful due to parasitoid competition. The coexistence of multiple parasitoids also affects the population dynamics. For instance, population oscillations can be removed by the introduction of a second parasitoid. In general, subtle differences in parasitoid phenology can give rise to different outcomes in a host–multi-parasitoid system, and this may offer some insight into why establishing criteria for the ‘ideal’ biological control agent has been so challenging.     

Evaluation of natural enemies for biological control: A behavioral approach

The success of biological pest control has stimulated the development of analytical models that explore the dynamics of natural enemies and their hosts or prey. These models seek to identify those general characteristics o f the natural enemy, host or prey population that lead to economic pest control. Because the models are strategic in nature, they are of limited value in identifying the specific attributes of an effective biological control agent prior to its introduction. Empirically developed criteria have also been of limited predictive value because they too provide only general guidelines. Behavioral ecology and foraging and sexratio theories may be useful adjuncts to these approaches, by identifying the evolutionary constraints and thus helping to define better the attributes of an effective natural enemy.     

Ship rat demography and diet following possum control in a mixed podocarp–hardwood forest

Control of one pest species may permit increases in abundance of other pests, thereby reducing the overall net benefit from pest control. We provide evidence that control of introduced possums (Trichosurus vulpecula) may increase ship rat (Rattus rattus) abundance in some New Zealand native forests. Ship rat abundance in a podocarp–hardwood forest was assessed using simple interference indices over 14 years (1990–2004) that included two aerial possum-poisoning operations (1994, 2000). Ship rat demography and rat and possum diet were measured from June 2001 to June 2003 when the rat population was increasing after the 2000 poisoning. Mean ship rat abundance indices increased nearly fivefold after possum control and remained high for up to 6 years after the 1994 poisoning. Rat fecundity was high (50–100% of adult females breeding), even during winter, and young animals dominated the population (73% in age classes 1–3) in 2001–2002 when rat numbers were increasing. During 2002–2003, rat abundance stabilised, without marked winter or spring reductions, the population aged significantly (only 32% in age classes 1–3), and fecundity declined to low levels (4–27% of adult females breeding). Although seeds and fruit dominated the diet of rats driving population recovery after control (74.0% of total diet by dry weight), rat fecundity was instead closely correlated with the proportional consumption of invertebrates (r = 0.91). Juvenile survival was correlated with proportional seed consumption (r = 0.75), while adult survival was correlated with combined seed and invertebrate consumption (r = 0.83). Adult rats ate more seeds and fewer invertebrates than juvenile rats. Seeds and fruit also dominated possum diet (52.2% of total diet). These results are consistent with the hypothesis that increased rat abundance following possum control is a consequence of greater availability of, or reduced competition for, seeds and fruit.     

Synergizing biological control: Scope for sterile insect technique,induced plant defences and cultural techniques to enhance natural enemy impact

When used alone, only a minority of biological control programs succeed in bringing the target pest population under sufficient control. Biological control is, therefore, usually employed with chemical, cultural, genetic or other methods in an integrated pest management (IPM) strategy. The interactions between different pest management methods, especially conventional pesticides and host plant resistance, is an area of growing research interest but relatively little consideration is given to novel combinations. This paper reviews the interactions between biological control and other forms of pest management, especially induced plant defences and the novel, non-toxic plant protection compounds that may boost these defences; and sterile insect technique. We also cover the cultural methods that offer scope to support synergies between the aforementioned methodological combinations. We conclude that despite the sometimes negative consequences of other pest management techniques for biological control efficacy, there is great scope for new strategies to be developed that exploit synergies between biological control and various other techniques. Ultimately, however, we propose that future use of biological control will involve integration at a greater conceptual scale such that this important form of pest management is promoted as one of a suite of ecosystem services that can be engineered into farming systems and wider landscapes.     

Bacterial Community Survey of Solenopsis invicta Buren (Red imported fire Ant) Colonies in the Presence and Absence of Solenopsis invicta Virus (SINV)

Insect bacterial symbionts contribute to many essential biological functions of their hosts and can also influence host fecundity and fitness. The physiological contribution symbionts provide can aid in immune response and xenobiotic detoxification. Both of these immune factors can directly impact strategies aimed at managing insect populations. One biological control strategy that shows promise in insects is the use of single-stranded RNA viruses within the group Dicistroviridae. The Solenopsis invicta Virus (SINV; Dicistroviridae), a ssRNA virus, has been proposed as a potential biological control agent for the urban pest S. invicta Buren or red imported fire ant (RIFA). SINV has been shown to be prevalent in RIFA populations of Texas and Florida; however, mortality is associated with high viral load. In other insect microbe systems, presence of particular bacteria induced resistance against Dicistrovirus. If this type of relationship is present in the RIFA–SINV system, their bacterial community could reduce the effectiveness of SINV as a biological control system. The advantage of 454 pyro-sequencing is that it enables classification of unculturable bacteria. This study examines the bacterial community in brood, workers, and reproductive cast members from colonies with and without SINV infection. Manipulation of the bacterial community may alter virus infection and replication within the mid-gut. Understanding the differences in the microbial community of ant colonies may provide insights that will refine current efforts designing control strategies for this important urban pest.     

The role of parasites in the dynamics of a reindeer population

Even though theoretical models show that parasites may regulate host population densities, few empirical studies have given support to this hypothesis. We present experimental and observational evidence for a host-parasite interaction where the parasite has sufficient impact on host population dynamics for regulation to occur. During a six year study of the Svalbard reindeer and its parasitic gastrointestinal nematode Ostertagia gruehneri we found that anthelminthic treatment in April-May increased the probability of a reindeer having a calf in the next year, compared with untreated controls. However, treatment did not influence the over-winter survival of the reindeer. The annual variation in the degree to which parasites depressed fecundity was positively related to the abundance of O. gruehneri infection the previous October, which in turn was related to host density two years earlier. In addition to the treatment effect, there was a strong negative effect of winter precipitation on the probability of female reindeer having a calf. A simple matrix model was parameterized using estimates from our experimental and observational data. This model shows that the parasite-mediated effect on fecundity was sufficient to regulate reindeer densities around observed host densities.     

Factors affecting parasitism by Microctonus aethiopoides (Hymenoptera: Braconidae) and parasitoid development in natural and novel host species

A laboratory study of aspects of parasitoid host acceptance, suitability and physiological regulation in natural and novel host species was carried out to investigate the degree of variability encountered with different hosts and to determine the value of such observations in host range determination. The parasitoid Microctonus aethiopoides Loan was exposed to a natural host, Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) and three novel hosts, the New Zealand native Nicaeana cervina Broun, the introduced weed biological control agent Rhinocyllus conicus (Froehlich), and a congeneric pest species, Sitona lepidus Gyllenhal (all Coleoptera: Curculionidae). Per cent parasitism of these species was 54%, 43%, 39% and 0%, respectively. The results indicated that for both S. discoideus and R. conicus more males than females were parasitized (69% cf. 45%, and 49% cf. 32% respectively) but host size was not a significant factor. Overall, superparasitism was recorded in about 29% of parasitized weevils and there was evidence that host discrimination to avoid superparasitism occurred in the natural host. Conversely, superparasitism occurred more frequently than would be expected in N. cervina (42%) coupled with higher survival of larvae in superparasitized hosts in this species. The frequency distribution of attack of R. conicus by M. aethiopoides was not different from random. Parasitoid development was more rapid in the natural host, S. discoideus, and parasitoid size was positively correlated with host size. There was a strong positive relationship between parasitoid larval survival and the presence of teratocytes in all hosts. Host fecundity and fertility were reduced by parasitism for most species, and in some cases, by exposure to parasitoids in the absence of detectable parasitism. It was concluded that laboratory observations can provide useful information on the compatibility between host and parasitoid which can complement traditional host range tests to predict field host range.     

Heligmosomoides polygyrus (Nematoda): the dynamics of primary and repeated infection in outbred mice

The population dynamics of Heligmosomoides polygyrus were studied in outbred male MF1 mice subject either to primary or repeated experimental infection. Little variability in susceptibility was observed between mice, but heterogeneity increased with both duration and intensity of primary infection; this result indicates that there are differences in parasite survival between hosts. The rate of parasite-induced host mortality was 4 X 10(-4) per parasite per host per parasite lifespan. The mortality rates of male and female larvae during their development in the intestinal wall were estimated as 0.033 and 0.021 per parasite per day respectively, and estimates of the expected lifespans of the adult male and female parasites in primary infection of 11.22 and 9.92 weeks were obtained. Approximately 40% of female worms were observed in copula at any one time, although this proportion was significantly depressed in hosts harbouring fewer than 50 parasites and during the first four weeks of infection. Parasite fecundity was markedly age-dependent; each female worm produced approximately 31,000 eggs during its lifespan. No density dependence in either worm survival or fecundity in primary infection was apparent. The only detectable effect of worm density was in association with spatial distribution in the intestine; high levels of infection were associated with a posterior shift in the location of a proportion of the parasite population. Characterization of the dynamics of primary infection allowed predictions to be made about the expected dynamics of repeated infection. The comparison of predicted results and observed data revealed unequivocal epidemiological evidence for the density-dependent regulation of parasite population growth during repeated infection, affecting both parasite survival and parasite fecundity. The results also demonstrated the existence of two types of host individual in which the dynamics of repeated infection were markedly different. It is concluded that immunological differences between mice (possibly under genetic control) may be responsible for the observed effects; approximately 25% of MF1 mice seem unable to generate any protective immunity against H. polygyrus, whereas 75% become almost completely refractory to reinfection. This experimental system could be used for quantitative investigation of the impact of acquired immunity and genetic heterogeneity on helminth population dynamics. Both are of obvious relevance with respect to the control of infections of medical and veterinary significance.     

Use of parasite regulation of host endocrinology to enhance the potential of biological control

The implications of parasite regulation of host endocrinology for successful biological control have not been fully appreciated. Insect parasites regulate host metamorphosis in a number of different ways. For a given host (pest) situation, each form of host regulation has its own advantages and disadvantages. Careful selection of a parasite based upon its mode lf host regulation can enhance the potential for biological control success. A basic knowledge of the endocrine basis for parasite regulation of its host will enable prediction of whether a parasite can regulate, and survive in, a host to which it has not been previously exposed.     

Argentine stem weevil ( Listronotus bonariensis, Coleoptera: Curculionidae) population dynamics in Canterbury, New Zealand dryland pasture

The Argentine stem weevil (Listronotus bonariensis) was an economically important pest in New Zealand pastures until the release of the parasitoid Microctonus hyperodae. This contribution uses historical data to investigate the regulation of the pest populations prior to, and somewhat during, the establishment of this parasitoid in dryland Canterbury, New Zealand. Thus, a significant goal of this study is to provide an L. bonariensis population dynamics baseline for any future work that aims to analyse the full effects of M. hyperodae on the weevil, now that equilibrium with the weevil host has been reached.The population dynamics of L. bonariensis, based on a life-table approach, were investigated using data collected regularly for eight years from populations in Canterbury, New Zealand. The key factor affecting end-of-season L. bonariensis density was found to be variation in second generation fourth instar prepupal and pupal mortality. This may have been caused by arrested development and ongoing mortality resulting from the onset of cooler autumnal conditions.A compensatory response was found in recruitment to the second summer weevil generation, whereby the realised fecundity of the emergent first summer generation of weevils was found to be negatively related to the density of adult weevils per ryegrass tiller. This is the first time that this has been found via long-term population analysis of L. bonariensis, although indications of this have been found elsewhere in caging, pot and small plot experiments.In this study, the effect of the parasitoid biocontrol agent Microctonus hyperodae on L. bonariensis population dynamics was unclear, as the analysis covered a period when the parasitoid Microctonus hyperodae was introduced and still establishing. It does, however, raise important questions for future analysis in terms of the interaction between parasitism and unrealised fecundity.The results in this contribution also highlighted regional differences. Overwintering mortality of adult weevils in Canterbury was constant between years, whilst earlier studies in the North Island Waikato region indicated this mortality was density dependent. In addition, the availability of tillers in endophyte-free ryegrass pastures in Canterbury had no influence on egg and early-instar larval survival, which contrasts with the finding from endophytic Waikato pastures.