duo to more perfect adaptatio.i and therefore more advanced 

 evolution. 



It is, as a matter of fact, probable that the migration is 

 primitive for some worms and secondarily acquired for others. 

 Worms which may be assumed normally to develop directly in 

 the intestine are at least occasionally able to reach the in 

 testine even if injected under the skin. This was demon- 

 strated by Harwood (1930) in tlie case Cosiiioccrcoidcs diikac, 

 for although he found the larvae of this worm to be incapable 

 of skin penetration, he succeeded in recovering a few worms 

 from lungs and intestine after subcutaneous injection. There 

 is some reason to believe that the Strongyloididae and Rhab- 

 diasidae, the latter of which never establish themselves in the 

 intestine at all, may be primitively skin penetrators, whereas 

 it is very unlikely that the ascarids are. Whether parenteral 

 migration is primitive or secondary among the Strongylina is 

 not so easy to guess. 



An interesting derivative of the migratory type of life cycle 

 is the course of develoi)ment of TricliinclUi. Th? unique life 

 cycle of this worm has apparently resulted from a precocious 

 development and hatching of the eggs in the uterus of the 

 mother, accompanied by early acquisition of the burrowing 

 instinct, the result being the invasion of the parental host in- 

 stead of a new host. The Strongylokles life cycle is another 

 derivative in which the parasitic worms have become partheno- 

 genetic and a free-living sexually-reproducing generation may 

 be interpolated in the course of a cycle of development whicli 

 is otherwise similar to that of hookworms. 



In the case of nematodes whose larvae hatch outside the 

 body and have an instinct for burrowing it is easy to conceive 

 of the accidental or, in time, routine invasion of intermediate 

 or transport hosts. This might come about by invasion from 

 the outside (e.g., Protostrongylinae), or by penetration through 

 the gut wall after being swallowed (e.g., Anisakinae). Such 

 penetration of hosts other than the definitive one, and subse- 

 quent encapsulation in parenteral tissues, is an extremely com- 

 mon phenomenon, and occurs in all the major groups of para- 

 sitic nematodes. In some instances it is a more or less ex- 

 ceptional phenomenon, e.g., the encystment of Tojcocuia larvae 

 in mice (Fiilleborn, IH21) ; in others it constitutes an im- 

 portant but not absolutely essential factor in the epidemiology, 

 e.g., Syngamun trachea; and in still others it has become ob- 

 ligatory, the invaded hosts then becoming true intermediate 

 hosts rather than transport hosts, e.g., spiruroids. 



The frequent encapsulation of some nematodes in transport 

 hosts and its non -occurrence in others is i)robably dependent 

 upon the behavior of the larvae in the hosts concerned. Larvae 

 that keep on the move do not become encapsulated. It is 

 for this reason that most spiruroids are encapsulated, whereas 

 Habioncma and filariae are not. No encapsulation of hook- 

 worm or Ascaris liimbricoides larvae occurs when these enter 

 rodents since the larvae complete the migration to the intes- 

 tine, and are then evacuated because the environment is un- 

 suitable for growth to maturity. On the other hand, since 

 Toxocara is encapsulated in mice, it must be assumed that this 

 worm loses its burrowing instinct before it has regained the 

 alimentary canal, and then becomes quiet enough to be en- 

 capsulated by the host. 



In the Metastrongylidae alone all gradations can be found 

 from more or less accidental and unnecessary penetration of 

 an intermediate host (e.g., Dictyocaulus filaria) to obligatory 

 development in specific invertebrates (e.g., Aleta.stroiipyhiK. 

 Protostrongylus and Muellerius). Similar obligatory depend- 

 ence upon specific intermediate hosts has become the lot of 

 the entire group of spiruroids, the C'amallanina, the Diocto- 

 phymatina, and apparently at least one ascaridoid, SiibiiUira 

 hrumpti (Alieata, 1939). 



A clue to the origin of the iilarioid type of life cycle, in 

 which the microfilariae are withdrawn from blood or skin 

 by blood sucking arthropods, and are eventually given an 

 opportunity for reinvasion of the skin by these same arthro- 

 pods, after development within them, is afforded by the 

 habronemas (see p. 286). In these the larvae show a definite 

 step towards the filarial type in that they fail to become 

 encapsulated in the intermediate host, there to await passive 

 transfer to the definite host, but instead remain free and 

 active, and leave the intermediate host, under suitable con- 

 ditions, of their own volition. The further steps to a filarial 

 life cycle are merely (1) substitution of a parenteral for a 

 gastrointestinal habitat for the adult worms, and consequent 

 liberation of the embryos into the blood or tissues whence 

 blood-sucking insects can withdraw them; and (2) successful 

 penetration of the skin by the infective larvae to reach their 

 deiinitive location. 



It will be seen that in no case is there reason to believe 

 that intermediate hosts of nematodes are ancestral hosts, as is 

 the case with intermediate hosts of flukes. 



The same modifications in life cycle have a tendency to re- 

 appear over and over again in the various groups of para- 



sitic nematodes, and sometimes several of the principal types 

 may occur within a group of closely related genera. In the 

 genus Habroncma, for instance, the species parasitic in the 

 stomachs of horses are deposited by the intermediate hosts 

 on the lips or skin and they reach their destination by way 

 of the mouth, either by direct migration into it or by being 

 licked from the skin. In the habronemas parasitic in insec- 

 tivorous birds, on the other hand, there can be little doubt 

 but that they reach their destination in the orthodox spiruroid 

 fashion, by the intermediate hosts harboring them being 

 swallowed. In the species found in raptorial birds, however, 

 a secondary transport host is usually if not always involved. 

 Because of this lack of uniformity within even nearly related 

 forms, and because of the endless number of minor varia- 

 tions by which one type of life cycle grades into another, 

 we believe that a clearer picture of the life cycles of parasitic 

 nematodes can be given by discussing the outstanding types 

 and principal variations in each natural group, than by dis- 

 cussing types of life cycles irrespective of the natural groups 

 in which they occur. By way of summary, however, we sug- 

 gest the following classification of the principal life cycle 

 types : 



A. Monoxenous or Direct (no intermediate host required). 



1. Continuous reproduction within host, generation after 

 generation ; various stages of worms occasionally carried 

 out of bod.v and infect other hosts through contaminated 

 food. Ex., Probstmayiia ; facultative rhabditoid para- 

 sites. 



2. Discontinuous, eggs or embryos escaping habitat of 

 adults, and usuall.v leaving parental host. 



(1) Without free-living phase. 



a. Simple. Eggs leave body of host, usually l)Ccoming 

 embryonated outside, reenter via the mouth usually 

 before hatching, and grow to maturity in the ali- 

 mentary canal. Ex., Enterobius, Trichiirin. 



h. With temporary burrowing into mucosa. Ex., 

 A scar id ia. 



c. With parenteral migration via blood system to heart 

 and lungs, returning to intestine via throat. Ex., 

 Ascaris laiiibricoidcs. 



d. With parenteral migration via blood system to 

 definitive locations elsewhere in body. Ex., Capil- 

 laria hepatica. 



(2) With free-living phase. Eggs usually hatch out- 

 side body of host into first-stage larvae which grow to 

 third (infective) stage while free, but in some forms 

 may develop to third stage before hatching. 



a. With skin ])enctration and migration to intestinal 

 tract via heart and lungs. 



(a) Free-living forms larvae only. Ex., Necator. 



(b) With possilile development of an alternative 

 generation of free-living adult males and fe- 

 males. Ex., Strongyloides. 



b. Without skin penetration; infection by mouth. 



(a) With temporary burrowing of larvae into 

 mucosa. Ex., Ilaeinonchiis. 



(b) With more extended burrowing and forma- 

 tion of nodules in intestinal wall. Ex., 

 Oesophagoslomii III. 



(c) Migration through intestinal wall and for- 

 mation of nodules in parenteral locations. 

 Ex., Strongyhis. 



c. With optional use of transport host. Infective 

 larvae when ingested by various invertebrates be- 

 come enc.vsted and reach final host when trans- 

 port host is eaten. Ex., Syngamus ; Dictyocaulus. 



B. Heteroxenous or Indirect (development occurs only in 



an intermediate host) 



1. Passive Indirect. Embryonated eggs or larvae enter 

 an intermediate host and become infective upon reach- 

 ing third stage. Pinal host reached when intermediate 

 host is eaten. Migration in definitive host, if any, via 

 tissues or natural passages, not via blood system. 



(1) Eggs cr larvae leave host with feces. 



a. Embryonated eggs or larvae are swallowed by 

 intermediate host. Ex., MetasiroiigyUis, spiruroids. 



b. Larvae superficially penetrate foot of molluscs. Ex., 

 Protostrongylinae. 



(2) Larvae leave host through skin or by other paren- 

 teral routes. Develop after being swallowed by in 

 termediate host. Ex., Dracunculoidea. 



2. Active Indirect. Larvae actively leave intermediate host 

 to reach skin of definitive host. 



(1) Larvae reach intermediate host by eggs being eaten. 

 Ex., Habroncma. 



(2) Larvae reach intermediate host by being sucked 

 from blood or skin. Ex., Filariae. 



3. Double Indirect. Larvae utilize two or more succes- 

 sive intermediate hosts. 



268 



